Structural bases of hydrogen tunneling in enzymes: Progress and puzzles

Current Opinion in Structural Biology

Volumn 14, Issue 6, 2004, Pages 648-655

  Liang, Zhao Xun ^a   Klinman, Judith P ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALCOHOL DEHYDROGENASE; DIHYDROFOLATE REDUCTASE; ENZYME; HYDROGEN; LIPOXYGENASE;

BIOCHEMISTRY; CATALYSIS; CHEMICAL REACTION; COMPARATIVE STUDY; ENERGY; ENZYME ACTIVITY; MUTATION; OXIDATION; PRIORITY JOURNAL; PROTON TRANSPORT; QUANTUM CHEMISTRY; REDUCTION; REVIEW; SIMULATION; SOYBEAN; SPECTROMETRY; STRUCTURE ANALYSIS; TEMPERATURE MEASUREMENT;

ALCOHOL DEHYDROGENASE; ANIMALS; BIOLOGICAL TRANSPORT; CATALYSIS; ENZYME ACTIVATION; ENZYMES; HUMANS; HYDROGEN; KINETICS; LIPOXYGENASE; MODELS, BIOLOGICAL; MODELS, CHEMICAL; MODELS, MOLECULAR; PROTEIN CONFORMATION; STRUCTURE-ACTIVITY RELATIONSHIP; TETRAHYDROFOLATE DEHYDROGENASE;

GLYCINE MAX;

EID: 9944236426     PISSN: 0959440X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.sbi.2004.10.008     Document Type: Review

References (63)

1. R.A. Marcus, and N. Sutin Electron transfers in chemistry and biology Biochim Biophys Acta 811 1985 265 322
2. M. Bixon, and J. Jortner Electron transfer - from isolated molecules to biomolecules, Pt 1 Adv Chem Phys 106 1999 35 202
3. H.B. Gray, and J.R. Winkler Electron tunneling through proteins Q Rev Biophys 36 2003 341 372
4. V.I. Goldanskii Chemical reactions at very low temperatures Annu Rev Phys Chem 27 1976 85 126
5. V.A. Benderskii, V.I. Goldanskii, and D.E. Makarov Quantum dynamics in low-temperature chemistry Phys Rep 233 1993 195 339
6. R.P. Bell The Proton in Chemistry edn 2 1973 Cornell University Press New York
7. R.P. Bell The Tunnel Effect in Chemistry 1980 Chapman and Hall New York
8. Y. Cha, C.J. Murray, and J.P. Klinman Hydrogen tunneling in enzyme reactions Science 243 1989 1325 1330
9. K.L. Grant, and J.P. Klinman Evidence that both protium and deuterium undergo significant tunneling in the reaction catalyzed by bovine serum amine oxidase Biochemistry 28 1989 6597 6605
10. S.L. Seymour, and J.P. Klinman Comparison of rates and kinetic isotope effects using PEG-modified variants and glycoforms of glucose oxidase: the relationship of modification of the protein envelope to C-H activation and tunneling Biochemistry 41 2002 8747 8758
11. W.A. Francisco, M.J. Knapp, N.J. Blackburn, and J.P. Klinman Hydrogen tunneling in peptidylglycine alpha-hydroxylating monooxygenase J Am Chem Soc 124 2002 8194 8195 In comparison to SLO-1, the hydrogen atom transfer catalyzed by peptidylglycine α-hydroxylating monooxygenase (PHM) exhibits very different activation and tunneling parameters. The differences were attributed to the increased solvent exposure and flexibility of the PHM active site.
12. G. Maglia, and R.K. Allemann Evidence for environmentally coupled hydrogen tunneling during dihydrofolate reductase catalysis J Am Chem Soc 125 2003 13372 13373
13. J. Basran, R.J. Harris, M.J. Sutcliffe, and N.S. Scrutton H-tunneling in the multiple H-transfers of the catalytic cycle of morphinone reductase and in the reductive half-reaction of the homologous pentaerythritol tetranitrate reductase J Biol Chem 278 2003 43973 43982 In pentaerythritol tetranitrate reductase, the KIE for hydride transfer is essentially independent of temperature in the experimentally accessible range. This contrasts with strongly temperature-dependent reaction rates and is consistent with a tunneling mechanism from the vibrational ground state of the reactive C-H/D bond.
14. N. Agrawal, B.Y. Hong, C. Mihai, and A. Kohen Vibrationally enhanced hydrogen tunneling in the Escherichia coli thymidylate synthase catalyzed reaction Biochemistry 43 2004 1998 2006
15. R.S. Sikorski, L. Wang, K.A. Markham, Rajagopalan PTR, S.J. Benkovic, and A. Kohen Tunneling and coupled motion in the Escherichia coli dihydrofolate reductase catalysis J Am Chem Soc 126 2004 4778 4779
16. A. Kohen, and J.P. Klinman Enzyme catalysis: beyond classical paradigms Acc Chem Res 31 1998 397 404
17. M.J. Knapp, and J.P. Klinman Environmentally coupled hydrogen tunneling - linking catalysis to dynamics Eur J Biochem 269 2002 3113 3121
18. M.J. Sutcliffe, and N.S. Scrutton A new conceptual framework for enzyme catalysis - hydrogen tunneling coupled to enzyme dynamics in flavoprotein and quinoprotein enzymes Eur J Biochem 269 2002 3096 3102
19. D. Antoniou, S. Caratzoulas, C. Kalyanaraman, J.S. Mincer, and S.D. Schwartz Barrier passage and protein dynamics in enzymatically catalyzed reactions Eur J Biochem 269 2002 3103 3112
20. S.J. Benkovic, and S. Hammes-Schiffer A perspective on enzyme catalysis Science 301 2003 1196 1202
21. J.P. Klinman Dynamic barriers and tunneling. New views of hydrogen transfer in enzyme reactions Pure Appl Chem 75 2003 601 608
22. M.J. Knapp, F.P. Seebeck, and J.P. Klinman Steric control of oxygenation regiochemistry in soybean lipoxygenase-1 J Am Chem Soc 123 2001 2931 2932
23. M.H. Glickman, J.S. Wiseman, and J.P. Klinman Extremely large isotope effects in the soybean lipoxygenase-linoleic acid reaction J Am Chem Soc 116 1994 793 794
24. T. Jonsson, M.H. Glickman, S.J. Sun, and J.P. Klinman Experimental evidence for extensive tunneling of hydrogen in the lipoxygenase reaction: implications for enzyme catalysis J Am Chem Soc 118 1996 10319 10320
25. E.N. Segraves, and T.R. Holman Kinetic investigations of the rate-limiting step in human 12- and 15-lipoxygenase Biochemistry 42 2003 5236 5243
26. M.J. Knapp, K. Rickert, and J.P. Klinman Temperature-dependent isotope effects in soybean lipoxygenase-1: correlating hydrogen tunneling with protein dynamics J Am Chem Soc 124 2002 3865 3874 The effect of a series of active site mutations on the magnitude of the H/D KIE and the temperature dependence of the KIE was studied. An expanded Marcus-like model was presented to account for the observed effects. The experimental parameters, which included the energy of activation, and the magnitude and temperature dependences of the KIE, could be fit by the model.
27. A.M. Kuznetsov, and J. Ulstrup Proton and hydrogen atom tunneling in hydrolytic and redox enzyme catalysis Can J Chem 77 1999 1085 1096
28. N. Lehnert, and E.I. Solomon Density-functional investigation on the mechanism of H-atom abstraction by lipoxygenase J Biol Inorg Chem 8 2003 294 305
29. E. Hatcher, A.V. Soudackov, and S. Hammes-Schiffer Proton-coupled electron transfer in soybean lipoxygenase J Am Chem Soc 126 2004 5763 5775 A theoretical study of the PCET reaction (hydrogen atom transfer) in SLO-1 with a multistate continuum model. The simulations provided insight into the large magnitude KIE, as well as the temperature dependence of hydrogen transfer rates and KIEs.
30. M.M. Olsson, P.E.M. Siegbahn, and A. Warshel Simulations of the large kinetic isotope effect and the temperature dependence of the hydrogen atom transfer in lipoxygenase J Am Chem Soc 126 2004 2820 2828
31. B.J. Bahnson, D. Park, K. Kim, B.V. Plapp, and J.P. Klinman Unmasking of hydrogen tunneling in the horse liver alcohol dehydrogenase reaction by site-directed mutagenesis Biochemistry 32 1993 5503 5507
32. W.H. Saunders Calculations of isotope effects in elimination-reactions - new experimental criteria for tunneling in slow proton transfers J Am Chem Soc 107 1985 164 169
33. B.J. Bahnson, T.D. Colby, J.K. Chin, B.M. Goldstein, and J.P. Klinman A link between protein structure and enzyme catalyzed hydrogen tunneling Proc Natl Acad Sci USA 94 1997 12797 12802
34. S.R. Billeter, S.P. Webb, P.K. Agarwal, T. Iordanov, and S. Hammes-Schiffer Hydride transfer in liver alcohol dehydrogenase: quantum dynamics, kinetic isotope effects, and role of enzyme motion J Am Chem Soc 123 2001 11262 11272
35. S. Caratzoulas, J.S. Mincer, and S.D. Schwartz Identification of a protein-promoting vibration in the reaction catalyzed by horse liver alcohol dehydrogenase J Am Chem Soc 124 2002 3270 3276 This computational study found that the hydride transfer coordinate is coupled with substrate-NAD motion. From the fact that the coupling vanishes at or near the transition state, it was concluded that substrate-NAD motion plays the role of a promoting vibration, symmetrically coupled to the reaction coordinate.
36. J.S. Mincer, and S.D. Schwartz A computational method to identify residues important in creating a protein promoting vibration in enzymes J Phys Chem B 107 2003 366 371
37. A. Kohen, R. Cannio, S. Bartolucci, and J.P. Klinman Enzyme dynamics and hydrogen tunnelling in a thermophilic alcohol dehydrogenase Nature 399 1999 496 499
38. J. Basran, M.J. Sutcliffe, and N.S. Scrutton Deuterium isotope effects during carbon-hydrogen bond cleavage by trimethylamine dehydrogenase. Implications for mechanism and vibrationally assisted hydrogen tunneling in wild-type and mutant enzymes J Biol Chem 276 2001 24581 24587
39. D. Antoniou, and S.D. Schwartz Internal enzyme motions as a source of catalytic activity: rate-promoting vibrations and hydrogen tunneling J Phys Chem B 105 2001 5553 5558
40. Z.X. Liang, T. Lee, K.A. Resing, N.G. Ahn, and J.P. Klinman Thermal activated protein mobility and its correlation with catalysis in thermophilic alcohol dehydrogenase Proc Natl Acad Sci USA 101 2004 9556 9561 This temperature-dependent study, using HX-MS, demonstrated that a local region in htADH adopts a more dynamic structure at elevated temperature. These studies provided support for the thermal-activated hydrogen tunneling model previously proposed based on kinetic data [37].
41. Liang Z-X, Tsigos I, Bouriotis V, Resing KA, Ahn NG, Klinman JP: Evidence for increased local conformational flexibility in psychrophilic alcohol dehydrogenase relative to its thermophilic homologue. Biochemistry 2004, in press.
42. Z.-X. Liang, I. Tsigos, V. Bouriotis, and J.P. Klinman Impact of protein flexibility on hydride transfer parameters in thermophilic and psychrophilic alcohol dehydrogenases J Am Chem Soc 126 2004 9500 9501
43. J.R. Schnell, H.J. Dyson, and P.E. Wright Structure, dynamics, and catalytic function of dihydrofolate reductase Annu Rev Biophys Biomol Struct 33 2004 119 140
44. S. Hammes-Schiffer Impact of enzyme motion on activity Biochemistry 41 2002 13335 13343
45. M.J. Osborne, J. Schnell, S.J. Benkovic, H.J. Dyson, and P.E. Wright Backbone dynamics in dihydrofolate reductase complexes: role of loop flexibility in the catalytic mechanism Biochemistry 40 2001 9846 9859
46. P.K. Agarwal, S.R. Billeter, and S. Hammes-Schiffer Nuclear quantum effects and enzyme dynamics in dihydrofolate reductase catalysis J Phy Chem B 106 2002 3283 3293
47. M. Garcia-Viloca, D.G. Truhlar, and J.L. Gao Reaction-path energetics and kinetics of the hydride transfer reaction catalyzed by dihydrofolate reductase Biochemistry 42 2003 13558 13575
48. P.K. Agarwal, S.R. Billeter, Rajagopalan PTR, S.J. Benkovic, and S. Hammes-Schiffer Network of coupled promoting motions in enzyme catalysis Proc Natl Acad Sci USA 99 2002 2794 2799 This study suggests the existence of a network of coupled protein motions maintained by conserved residues. This suggestion is based on sequence comparison and mixed quantum/classical molecular dynamics simulations of hydride transfer. The implication is that subtle mutations, distal from the active site, may disrupt this network and affect hydride transfer.
49. K.M. Doll, B.R. Bender, and R.G. Finke The first experimental test of the hypothesis that enzymes have evolved to enhance hydrogen tunneling J Am Chem Soc 125 2003 10877 10884 These data show that the hydrogen atom abstraction between ethylene glycol and a coenzyme B-12 derivative radical in solution exhibits similar KIEs and temperature-dependent behavior to the hydrogen atom transfer catalyzed by methylmalonyl-CoA mutase. Based on these observations, the authors concluded that the enzyme does not alter the properties of hydrogen tunneling.
50. K.M. Doll, and R.G. Finke A compelling experimental test of the hypothesis that enzymes have evolved to enhance quantum mechanical tunneling in hydrogen transfer reactions: the beta-neopentylcobalamin system combined with prior adocobalamin data Inorg Chem 42 2003 4849 4856
51. M.P. Valley, and P.F. Fitzpatrick Comparison of enzymatic and non-enzymatic nitroethane anion formation: thermodynamics and contribution of tunneling J Am Chem Soc 126 2004 6244 6245
52. C.R. Goldsmith, R.T. Jonas, and T.D. Stack C-H bond activation by a ferric methoxide complex modeling the rate-determining step in the mechanism of lipoxygenase J Am Chem Soc 124 2002 83 96
53. D.J. Heyes, A.V. Ruban, and C.N. Hunter Protochlorophyllide oxidoreductase: "dark" reactions of a light-driven enzyme Biochemistry 42 2003 523 528 The unique light-driven enzyme protochlorophyllide oxidoreductase allows the initiation of catalysis with illumination of pre-bound cofactor and substrate. The temperature dependence study showed that hydride transfer only occurs close to or above 200 K, indicating that protein dynamics are required for the hydrogen transfer reaction.
54. P. Faller, C. Goussias, A.W. Rutherford, and S. Un Resolving intermediates in biological proton-coupled electron transfer: a tyrosyl radical prior to proton movement Proc Natl Acad Sci USA 100 2003 8732 8735
55. T. Jonsson, D.E. Edmondson, and J.P. Klinman Hydrogen tunneling in the flavoenzyme monoamine oxidase B Biochemistry 33 1994 14871 14878
56. J.C. Nesheim, and J.D. Lipscomb Large kinetic isotope effects in methane oxidation catalyzed by methane monooxygenase: evidence for C-H bond cleavage in a reaction cycle intermediate Biochemistry 35 1996 10240 10247
57. M.M. Whittaker, D.P. Ballou, and J.W. Whittaker Kinetic isotope effects as probes of the mechanism of galactose oxidase Biochemistry 37 1998 8426 8436
58. J. Basran, M.J. Sutcliffe, and N.S. Scrutton Enzymatic H-transfer requires vibration-driven extreme tunneling Biochemistry 38 1999 3218 3222
59. S. Chowdhury, and R. Banerjee Evidence for quantum mechanical tunneling in the coupled cobalt-carbon bond homolysis-substrate radical generation reaction catalyzed by methylmalonyl-CoA mutase J Am Chem Soc 122 2000 5417 5418
60. R.J. Harris, R. Meskys, M.J. Sutcliffe, and N.S. Scrutton Kinetic studies of the mechanism of carbon-hydrogen bond breakage by the heterotetrameric sarcosine oxidase of Arthrobacter sp. 1-IN Biochemistry 39 2000 1189 1198
61. J.L. Abad, F. Camps, and G. Fabrias Is hydrogen tunneling involved in acylCoA desaturase reactions? The case of a delta(9) desaturase that transforms (E)-11-tetradecenoic acid into (Z,E)-9,11-tetradecadienoic acid Angew Chem (Int Ed) 39 2000 3279 3281
62. M. Garcia-Viloca, C. Alhambra, D.G. Truhlar, and J. Gao Quantum dynamics of hydride transfer catalyzed by bimetallic electrophilic catalysis: synchronous motion of Mg(2+) and H(-) in xylose isomerase J Am Chem Soc 124 2002 7268 7269
63. Q. Cui, and M. Karplus 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 2002 3093 3124