Structural and mechanistic aspects of flavoproteins: Probes of hydrogen tunnelling

FEBS Journal

Volumn 276, Issue 15, 2009, Pages 3930-3941

  Hay, Sam ^a   Pudney, Christopher R ^a   Scrutton, Nigel S ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

H tunneling; High pressure; Kinetic isotope effect; Kinetic isotope fractionation; Multiple reactive conformations; Old Yellow Enzyme; Promoting vibration; Protein dynamics; Quantum mechanics; Stopped flow kinetics

Indexed keywords

AMINE OXIDASE (FLAVIN CONTAINING) ISOENZYME A; AMINE OXIDASE (FLAVIN CONTAINING) ISOENZYME B; CHOLINE OXIDASE; DIHYDROOROTATE DEHYDROGENASE; FLAVINE MONONUCLEOTIDE; FLAVOPROTEIN; GLUCOSE OXIDASE; PENTAERYTHRITYL TETRANITRATE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE DEHYDROGENASE; SARCOSINE OXIDASE;

COENZYME; ELECTRON TRANSPORT; ENTEROBACTER CLOACAE; HYDROGEN TUNNELLING; HYDROSTATIC PRESSURE; NONHUMAN; PRIORITY JOURNAL; PROTON TRANSPORT; PSEUDOMONAS PUTIDA; QUANTUM MECHANICS; REGULATORY MECHANISM; SHORT SURVEY; STRUCTURAL PROTEOMICS; VISCOSITY;

AMINO ACID SEQUENCE; ANIMALS; ARABIDOPSIS; BINDING SITES; CARBOHYDRATES; ELECTRON-TRANSFERRING FLAVOPROTEINS; FLAVOPROTEINS; GLYCOGEN; HUMANS; MAMMALS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN CONFORMATION; SEQUENCE ALIGNMENT; STARCH;

EID: 68149157996     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2009.07121.x     Document Type: Short Survey

References (79)

1. Garcia-Viloca M, Gao J, Karplus M Truhlar DG (2004) How enzymes work: analysis by modern rate theory and computer simulations. Science 303, 186 195.
2. Cha Y, Murray CJ Klinman JP (1989) Hydrogen tunneling in enzyme-reactions. Science 243, 1325 1330.
3. Benkovic SJ Hammes-Schiffer S (2003) A perspective on enzyme catalysis. Science 301, 1196 1202.
4. Masgrau L, Roujeinikova A, Johannissen LO, Hothi P, Basran J, Ranaghan KE, Mulholland AJ, Sutcliffe MJ, Scrutton NS Leys D (2006) Atomic description of an enzyme reaction dominated by proton tunneling. Science 312, 237 241.
5. Kohen A, Cannio R, Bartolucci S Klinman JP (1999) Enzyme dynamics and hydrogen tunnelling in a thermophilic alcohol dehydrogenase. Nature 399, 496 499.
6. Antoniou D Schwartz SD (1997) Large kinetic isotope effects in enzymatic proton transfer and the role of substrate oscillations. Proc Natl Acad Sci USA 94, 12360 12365.
7. Caratzoulas S, Mincer JS Schwartz SD (2002) Identification of a protein-promoting vibration in the reaction catalyzed by horse liver alcohol dehydrogenase. J Am Chem Soc 124, 3270 3276.
8. Hay S, Sutcliffe MJ Scrutton NS (2007) Promoting motions in enzyme catalysis probed by pressure studies of kinetic isotope effects. Proc Natl Acad Sci USA 104, 507 512.
9. Johannissen LO, Hay S, Scrutton NS Sutcliffe MJ (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.
10. Knapp MJ Klinman JP (2002) Environmentally coupled hydrogen tunneling - linking catalysis to dynamics. Eur J Biochem 269, 3113 3121.
11. Antoniou D Schwartz SD (2001) Internal enzyme motions as a source of catalytic activity: rate-promoting vibrations and hydrogen tunneling. J Phys Chem B 105, 5553 5558.
12. Bruno WJ Bialek W (1992) Vibrationally enhanced tunneling as a mechanism for enzymatic hydrogen transfer. Biophys J 63, 689 699.
13. Basran J, Sutcliffe MJ Scrutton NS (1999) Enzymatic H-transfer requires vibration-driven extreme tunneling. Biochemistry 38, 3218 3222.
14. Basran J, Patel S, Sutcliffe MJ Scrutton NS (2001) Importance of barrier shape in enzyme-catalyzed reactions - vibrationally assisted hydrogen tunneling in tryptophan tryptophylquinone-dependent amine dehydrogenases. J Biol Chem 276, 6234 6242.
15. Basran J, Harris RJ, Sutcliffe MJ Scrutton NS (2003) 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, 43973 43982.
16. Basran J, Sutcliffe MJ Scrutton NS (2001) 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, 24581 24587.
17. Harris RJ, Meskys R, Sutcliffe MJ Scrutton NS (2000) Kinetic studies of the mechanism of carbon-hydrogen bond breakage by the heterotetrameric sarcosine oxidase of Arthrobacter sp 1-IN. Biochemistry 39, 1189 1198.
18. Pudney CR, Hay S, Sutcliffe MJ Scrutton NS (2006) Alpha-secondary isotope effects as probes of 'tunneling-ready' configurations in enzymatic H-tunneling: insight from environmentally coupled tunneling models. J Am Chem Soc 128, 14053 14058.
19. Pudney CR, Hay S, Pang JY, Costello C, Leys D, Sutcliffe MJ Scrutton NS (2007) Mutagenesis of morphinone reductase induces multiple reactive configurations and identifies potential ambiguity in kinetic analysis of enzyme tunneling mechanisms. J Am Chem Soc 129, 13949 13956.
20. Hay S, Pudney CR, Sutcliffe MJ Scrutton NS (2008) Are environmentally coupled enzymatic hydrogen tunneling reactions influenced by changes in solution viscosity? Angew Chem Int Ed Engl 47, 537 540.
21. Ball P (2004) Enzymes - by chance, or by design? Nature 431, 396 397.
22. Gladstone S, Laidler KJ Eyring H (1941) The Theory of Rate Processes. McGraw-Hill, New York, NY.
23. Marcus RA Sutin N (1985) Electron transfers in chemistry and biology. Biochim Biophys Acta 811, 265 322.
24. Devault D, Parkes JH Chance B (1967) Electron tunnelling in cytochromes. Nature 215, 642 644.
25. Pang J, Pu JZ, Gao JL, Truhlar DG Allemann RK (2006) 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.
26. Garcia-Viloca M, Truhlar DG Gao JL (2003) Reaction-path energetics and kinetics of the hydride transfer reaction catalyzed by dihydrofolate reductase. Biochemistry 42, 13558 13575.
27. Tejero I, Garcia-Viloca M, Gonzalez-Lafont A, Lluch JM York DM (2006) Enzyme dynamics and tunneling enhanced by compression in the hydrogen abstraction catalyzed by soybean lipoxygenase-1. J Phys Chem B 110, 24708 24719.
28. Pang J, Hay S, Scrutton NS Sutcliffe MJ (2008) Deep tunneling dominates the biologically important hydride transfer reaction from NADH to FMN in morphinone reductase. J Am Chem Soc 130, 7092 7097.
29. Brinkley DW Roth JP (2005) Determination of a large reorganization energy barrier for hydride abstraction by glucose oxidase. J Am Chem Soc 127, 15720 15721.
30. Hothi P, Hay S, Roujeinikova A, Sutcliffe MJ, Lee M, Leys D, Cullis PM Scrutton NS (2008) Driving force analysis of proton tunnelling across a reactivity series for an enzyme-substrate complex. ChemBioChem 9, 2839 2845.
31. Knapp MJ, Rickert K Klinman JP (2002) Temperature-dependent isotope effects in soybean lipoxygenase-1: correlating hydrogen tunneling with protein dynamics. J Am Chem Soc 124, 3865 3874.
32. Kuznetsov AM Ulstrup J (1999) Proton and hydrogen atom tunnelling in hydrolytic and redox enzyme catalysis. Can J Chem 77, 1085 1096.
33. Bell R (1980) The Tunnel Effect in Chemistry. Chapman and Hall, London.
34. Hay S, Pudney C, McGrory TA, Pan J, Sutcliffe MJ Scrutton NS (2009) Barrier compression enhances an enzymatic H-transfer reaction. Angew Chem 48, 1452 1454.
35. Craig DH, Moody PCE, Bruce NC Scrutton NS (1998) Reductive and oxidative half-reactions of morphinone reductase from Pseudomonas putida M10: a kinetic and thermodynamic analysis. Biochemistry 37, 7598 7607.
36. Huskey WP Schowen RL (1983) Reaction-coordinate tunneling in hydride-transfer reactions. J Am Chem Soc 105, 5704 5706.
37. Saunders WH (1985) Calculations of isotope effects in elimination-reactions - new experimental criteria for tunneling in slow proton transfers. J Am Chem Soc 107, 164 169.
38. + analogs. J Am Chem Soc 105, 7629 7631.
39. Hay S, Pudney CR, Hothi P Scrutton NS (2008) Correction of pre-steady state KIEs for isotopic impurities and the consequences of kinetic isotope fractionation. J Phys Chem A 112, 13109 13115.
40. Hay S, Pudney CR, Sutcliffe MJ Scrutton NS (2008) Solvent as a probe of active site motion and chemistry during the hydrogen tunnelling reaction in morphinone reductase. ChemPhysChem 9, 1875 1881.
41. Messiha HL, Munro AW, Bruce NC, Barsukov I Scrutton NS (2005) Reaction of morphinone reductase with 2-cyclohexen-1-one and 1-nitrocyclohexene. J Biol Chem 280, 10695 10709.
42. Khan H, Barna T, Bruce NC, Munro AW, Leys D Scrutton NS (2005) Proton transfer in the oxidative half-reaction of pentaerythritol tetranitrate reductase. FEBS J 272, 4660 4671.
43. Pudney CR, McGrory T, Lafite P, Pang J, Hay S, Leys D, Sutcliffe MJ Scrutton NS (2009) Parallel pathways and free-energy landscapes for enzymatic hydride transfer probed by hydrostatic pressure. ChemBioChem 10, 1379 1384.
44. Hay S, Pang JY, Monaghan PJ, Wang X, Evans RM, Sutcliffe MJ, Allemann RK Scrutton NS (2008) Secondary kinetic isotope effects as probes of environmentally-coupled enzymatic hydrogen tunneling reactions. ChemPhysChem 9, 1536 1539.
45. Cook PF, Blanchard JS Cleland WW (1980) Primary and secondary deuterium-isotope effects on equilibrium-constants for enzyme-catalyzed reactions. Biochemistry 19, 4853 4858.
46. Pu JZ, Ma SH, Garcia-Viloca M, Gao JL, Truhlar DG Kohen A (2005) Nonperfect synchronization of reaction center rehybridization in the transition state of the hydride transfer catalyzed by dihydrofolate reductase. J Am Chem Soc 127, 14879 14886.
47. Hay S Scrutton NS (2008) H-transfers in photosystem II: what can we learn from recent lessons in the enzyme community? Photosynth Res 98, 169 177.
48. Markham KA Kohen A (2006) Analytical procedures for the preparation, isolation, analysis and preservation of reduced nicotinamides. Curr Anal Chem 2, 379 388.
49. Viola RE, Cook PF Cleland WW (1979) Stereoselective preparation of deuterated reduced nicotinamide adenine-nucleotides and substrates by enzymatic-synthesis. Anal Biochem 96, 334 340.
50. McCracken JA, Wang T Kohen A (2004) Synthesis of R and S tritiated reduced beta-nicotinamide adenine dinucleotide 2′ phosphate. Anal Biochem 324, 131 136.
51. Ottolina G, Riva S, Carrea G, Danieli B Buckmann AF (1989) Enzymatic-synthesis of 4R-H-2NAD(P)H and 4S-H-2NAD(P)H and determination of the stereospecificity of 7-alpha-hydroxysteroid and 12-alpha-hydroxysteroid dehydrogenase. Biochim Biophys Acta 998, 173 178.
52. Branlant G, Eiler B Biellmann JF (1982) A word of caution - 1,4,5,6-tetrahydronicotinamide adenine-dinucleotide (phosphate) should be used with care in acidic and neutral media. Anal Biochem 125, 264 268.
53. Arnold LJ, You K, Allison WS Kaplan NO (1976) Determination of hydride transfer stereospecificity of nicotinamide adenine-dinucleotide linked oxidoreductases by proton magnetic-resonance. Biochemistry 15, 4844 4849.
54. Park H, Girdaukas GG Northrop DB (2006) Effect of pressure on a heavy-atom isotope effect of yeast alcohol dehydrogenase. J Am Chem Soc 128, 1868 1872.
55. Isaacs NS, Javaid K 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.
56. Isaacs NS (1984) The effect of pressure on kinetic isotope effects. In Isotope Effects in Organic Chemistry (Buncel E Lee CC eds pp. 67 105. Elsevier, London.
57. Isaacs NS, Javaid K Rannala E (1977) Pressure effects on proton tunnelling. Nature 268, 372.
58. Northrop DB (2006) Unusual origins of isotope effects in enzyme-catalysed reactions. Phil Trans R Soc Lond B Biol Sci 361, 1341 1349.
59. Northrop DB (1999) Effects of high pressure on isotope effects and hydrogen tunneling. J Am Chem Soc 121, 3521 3524.
60. Northrop DB (2002) Effects of high pressure on enzymatic activity. Biochim Biophys Acta 1595, 71 79.
61. Hay S, Sutcliffe MJ Scrutton NS (2009) Probing coupled motions in enzymatic hydrogen tunnelling reactions: beyond temperature-dependence studies of kinetic isotope effects. In Quantum Tunnelling in Enzyme Catalyzed Reactions (Allemann RK Scrutton NS eds pp. 199 218. Royal Society of Chemistry, London.
62. Hay S Scrutton NS (2008) Incorporation of hydrostatic pressure into models of hydrogen tunneling highlights a role for pressure-modulated promoting vibrations. Biochemistry 47, 9880 9887.
63. Ewald AH (1968) Effect of pressure on charge transfer complexes in solution. Trans Faraday Soc 64, 733 743.
64. von Smoluchowski M (1917) Mathematical theory of the kinetics of the coagulation of colloidal solutions. Z Phys Chem 92, 129 168.
65. Ansari A, Jones CM, Henry ER, Hofrichter J Eaton WA (1992) The role of solvent viscosity in the dynamics of protein conformational-changes. Science 256, 1796 1798.
66. Ivkovic-Jensen MM Kostic NM (1997) Effects of viscosity and temperature on the kinetics of the electron-transfer reaction between the triplet state of zinc cytochrome c and cupriplastocyanin. Biochemistry 36, 8135 8144.
67. Ivkovic-Jensen MM Kostic NM (1996) Effects of temperature on the kinetics of the gated electron-transfer reaction between zinc cytochrome c and plastocyanin. Analysis of configurational fluctuation of the diprotein complex. Biochemistry 35, 15095 15106.
68. Zhou JS Kostic NM (1993) Gating of photoinduced electron-transfer from zinc cytochrome-c and tin cytochrome-c to plastocyanin - effects of solution viscosity on rearrangement of the metalloprotein complex. J Am Chem Soc 115, 10796 10804.
69. Zhou JS Kostic NM (1992) Photoinduced electron-transfer from zinc cytochrome-c to plastocyanin is gated by surface-diffusion within the metalloprotein complex. J Am Chem Soc 114, 3562 3563.
70. Feng CJ, Kedia RV, Hazzard JT, Hurley JK, Tollin G Enemark JH (2002) Effect of solution viscosity on intramolecular electron transfer in sulfite oxidase. Biochemistry 41, 5816 5821.
71. Kohen A, Jonsson T Klinman JP (1997) Effects of protein glycosylation on catalysis: changes in hydrogen tunneling and enthalpy of activation in the glucose oxidase reaction. Biochemistry 36, 2603 2611.
72. Seymour SL Klinman JP (2002) 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, 8747 8758.
73. Ohta Y, Mukouyama EB Suzuki H (2006) Kinetic isotope effect of the l-phenylalanine oxidase from Pseudomonas sp P-501. J Biochem 139, 551 555.
74. Nagel ZD Klinman JP (2006) Tunneling and dynamics in enzymatic hydride transfer. Chem Rev 106, 3095 3118.
75. Fan F Gadda G (2005) Oxygen- and temperature-dependent kinetic isotope effects in choline oxidase: correlating reversible hydride transfer with environmentally enhanced tunneling. J Am Chem Soc 127, 17954 17961.
76. Dunn RV, Marshall KR, Munro AW Scrutton NS (2008) The pH dependence of kinetic isotope effects in monoamine oxidase A indicates stabilization of the neutral amine in the enzyme-substrate complex. FEBS J 275, 3850 3858.
77. Jonsson T, Edmondson DE Klinman JP (1994) Hydrogen tunneling in the flavoenzyme monoamine-oxidase-B. Biochemistry 33, 14871 14878.
78. Agrawal N, Lesley SA, Kuhn P Kohen A (2004) Mechanistic studies of a flavin-dependent thymidylate synthase. Biochemistry 43, 10295 10301.
79. Fagan RL, Nelson MN, Pagano PM Palfey BA (2006) Mechanism of flavin reduction in class 2 dihydroorotate dehydrogenases. Biochemistry 45, 14926 14932.