The role of tunneling in enzyme catalysis of C-H activation

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1757, Issue 8, 2006, Pages 981-987

  Klinman, Judith P ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON; HYDROGEN; ISOTOPE;

ATOM; CATALYSIS; DONOR; ELECTRON TRANSPORT; ENVIRONMENTAL FACTOR; ENZYME ACTIVE SITE; ENZYME KINETICS; NONHUMAN; PRIORITY JOURNAL; REACTION ANALYSIS; REVIEW; SITE DIRECTED MUTAGENESIS; TEMPERATURE DEPENDENCE;

AMINO ACID SEQUENCE; AMINO ACIDS; CATALYSIS; ELECTRON TRANSPORT; ENZYMES; HYDROGEN; KINETICS; PROTEIN CONFORMATION;

EID: 33748902041     PISSN: 00052728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbabio.2005.12.004     Document Type: Review

References (45)

1. Kurz L.C., and Frieden C. Anomalous equilibrium and kinetic alpha-deuterium secondary isotope effects accompanying hydride transfer from reduced nicotinamide adenine dinucleotide. J. Am. Chem. Soc. 102 (1980) 4198-4203
2. Cook P.F., Oppenheimer N.J., and Cleland W.W. Secondary deuterium and nitrogen-15 isotope effects in enzyme-catalyzed reactions. Chemical mechanism of liver alcohol dehydrogenase. Biochemistry 20 (1981) 1817-1825
3. Husky W.P., and Schowen R.L. Reaction-coordinate tunneling in hydride-transfer reactions. J. Am. Chem. Soc. 105 (1983) 5704-5706
4. Saunders Jr. W.H. Calculations of isotope effects in elimination reactions. New experimental criteria for tunneling in slow proton transfers. J. Am. Chem. Soc. 107 (1985) 164-169
5. Cha Y., Murray C.J., and Klinman J.P. Hydrogen tunneling in enzyme reactions. Science 243 (1989) 1325-1330
6. Bell R.P. The Tunneling Effect in Chemistry (1980), Chapman and Hall, New York, NY
7. Truhlar D.G., Isaacson A.D., and Garrett B.C. In: Baer M. (Ed). Theory of Chemical Reaction Dynamics vol. 4 (1985), CRC Press, Boca Raton, FL 65-137
8. Garcia-Viloca M., Gao J., Karplus M., and Truhlar D.G. How enzymes work: analysis by modern rate theory and computer simulations. Science 303 (2004) 186-195
9. Westheimer F.H. The magnitude of the primary kinetic isotope effect for compounds of hydrogen and deuterium. Chem. Rev. 61 (1961) 265-273
10. Kohen A., and Klinman J.P. Enzyme catalysis: beyond classical paradigms. Accts. Chem. Res. 31 (1998) 397-404
11. Kohen A., and Jensen J.H. Boundary conditions for the Swain-Schaad relationship as a criterion for hydrogen tunneling. J. Am. Chem. Soc. 124 (2002) 3858-3864
12. Hirschi J., and Singleton D.A. The normal range of secondary Swain-Schaad exponents without tunneling or kinetic complexity. J. Am. Chem. Soc. 127 (2005) 3294-3295
13. Grant K.L., and Klinman J.P. Evidence that both protium and deuterium undergo significant tunneling in the reaction catalyzed by bovine serum amine oxidase. Biochemistry 28 (1989) 6597-6605
14. Mure M., Mills S.A., and Klinman J.P. Catalytic mechanism of the topa quinone containing copper amine oxidase. Biochemistry 41 (2002) 9269-9278
15. Bruno W.J., and Bialek W. Vibrationally enhanced tunneling as a mechanism for enzymatic hydrogen transfer. Biophys. J. 63 (1992) 689-699
16. Levich V.G., Dogonadze R.R., German E.D., Kuznetsov A.M., and Kharkats Y.I. Theory of homogenous reactions involving proton transfer. Electrochim. Acta 15 (1970) 353-367
17. Marcus R.A., and Sutin N. Electron transfers in chemistry and biology. Biochim. Biophys. Acta 811 (1985) 265-322
18. Sutin N. Theory of electron transfer reactions: insights and hindsights. Prog. Inorg. Chem. 30 (1983) 441-498
19. Borgis D., and Hynes J.T. Dynamical theory of proton tunneling transfer sites in solution: general information. Chem. Phys. 170 (1993) 315-346
20. Kuznetsov A.M., and Ulstrup J. Proton and hydrogen atom tunneling in hydrolytic and redox enzyme catalysis. Can. J. Chem. 77 (1999) 1085-1096
21. Knapp M.J., Rickert K., and Klinman J.P. Temperature-dependent isotope effects in soybean lipoxygenase-1: correlating hydrogen tunneling with protein dynamics. J. Am. Chem. Soc. 124 (2002) 3865-3874
22. Knapp M.J., and Klinman J.P. Environmentally-coupled hydrogen tunneling: linking catalysis to dynamics. Eur. J. Biochem. 269 (2002) 3113-3121
23. Hatcher E., Soudackov A.V., and Hammes-Schiffer S. Proton-coupled electron transfer in soybean lipoxygenase. J. Am. Chem. Soc. 126 (2004) 5763-5775
24. Glickman M.H., Wiseman J.S., and Klinman J.P. Extremely large isotope effects in the soybean lipoxygenase-linoleic acid reaction. J. Am. Chem. Soc. 116 (1994) 793-794
25. Hwang C.C., and Grissom C.B. Unusually large deuterium isotope effects in soybean lipoxygenase are not caused by a magnetic isotope effect. J. Am. Chem. Soc. 116 (1994) 795-796
26. Rickert K.W., and Klinman J.P. The nature of hydrogen transfer in soybean lipoxygenase-1: separation of primary and secondary isotope effects. Biochemistry 38 (1999) 12218-12228
27. Segraves E.N., and Holman T.R. Kinetic investigations of the rate-limiting step in human 12- and 15-lipoxygenase. Biochemistry 42 (2003) 5236-5243
28. Meyer M., and Klinman J.P. 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 (2005) 283-296
29. M. Meyer, D. Tomchick, J.P. Klinman, Structure and dynamics among mutants of soybean lipoxygenase at position 553, (in preparation).
30. Roth J.P., Yoder J.C., Won T.-J., and Mayer J.M. Application of the Marcus cross reaction to hydrogen transfer reactions. Science 294 (2001) 2524-2526
31. Silverman D.N., Tu C., Chen X., Tanhauser S.M., Kresage A.J., and Laipus P.J. Rate-equilibria relationships in intramolecular proton transfer in human carbonic anhydrase 111. Biochemistry 32 (1993) 10757-10762
32. Kohen A., Cannio R., Bartolucci S., and Klinman J.P. Enzyme dynamics and hydrogen tunneling in a thermophilic alcohol dehydrogenase. Nature 399 (1999) 496-499
33. Basran J., Patel S., Sutcliffe M., and Scrutton N.S. Importance of barrier shape in enzyme-catalyzed reactions. Vibrationally assisted hydrogen tunneling in tryptophan tryptophylquinone-dependent amine dehydrogenases. J. Biol. Chem. 276 (2001) 6234-6242
34. Bahnson B.J., Colby T.D., Chin J.K., Goldstein B.M., and Klinman J.P. A link between protein structure and enzyme catalyzed hydrogen tunneling. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 12797-12802
35. Jonsson T., Edmondson D.E., and Klinman J.P. Hydrogen tunneling in the flavoenzyme monoamine oxidase. Biochemistry 33 (1994) 14871-14878
36. Seymour S.L., and Klinman J.P. Comparison of rates and kinetic isotope effects using PEG modified variants and glycoforms of glucose oxidases: the relationship of modification of the protein envelope to C-H activation in tunneling. Biochemistry 41 (2002) 8744-8758
37. Whittaker M.M., Ballou D.P., and Whittaker J.W. Kinetic isotope effects as probes of the mechanism of glucose oxidase. Biochemistry 37 (1998) 8426-8436
38. Chowdhury S., and Banerjee R. 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
39. Francisco W., Knapp M.J., Blackburn N.J., and Klinman J.P. Hydrogen tunneling in peptidylglycine-alpha hydroxylating monooxygenase. J. Am. Chem. Soc. 124 (2002) 8194-8195
40. Basran J., Sutcliffe M.J., and Scrutton N.S. Enzymatic H-transfer requires vibration-driven extreme tunneling. Biochemistry 38 (1999) 3218-3222
41. Basran J., Sutcliffe M.J., and Scrutton N.S. 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
42. Harris R.J., Meskys R., Sutcliffe M.J., and Scrutton N.S. 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
43. 9 desaturase that transforms (E)-11-tetradecenoic acid into (Z,E)-9-11 tetradecenoic acid. Angew. Chem., Int. Ed. 39 (2000) 3279-3281
44. Sikorski R.S., Wang L., Markham K.A., Ravi Rajagopalan P.T., Benkovic S.J., and Kohen A. Tunneling and coupled motion in the Escherichia coli dihydrofolate reduction catalysis. J. Am. Chem. Soc. 126 (2004) 4778-4779
45. Minor W., Steczko J., Stec B., Otwinowski Z., Bolin J.T., Walter R., and Axelrod B. Crystal structure of soybean lipoxygenase L-1 at 1.4 Å resolution. Biochemistry 35 (1996) 10687-10701