Reduction of ferric iron could drive hydrogen tunneling in lipoxygenase catalysis: Implications for enzymatic and chemical mechanisms

Journal of the American Chemical Society

Volumn 119, Issue 17, 1997, Pages 3853-3860

  Moiseyev, Nimrod ^a   Rucker, Joseph ^b   Glickman, Michael H ^c  

^a TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FERRIC ION; HYDROGEN; ISOTOPE; LIPOXYGENASE INHIBITOR; ORGANOMETALLIC COMPOUND;

ARTICLE; CATALYSIS; ELECTRON TRANSPORT; ENZYME ACTIVE SITE; ENZYME MECHANISM; PROTON TRANSPORT; QUANTUM MECHANICS; REDUCTION; SOYBEAN; TEMPERATURE DEPENDENCE;

EID: 0030920947     PISSN: 00027863     EISSN: None     Source Type: Journal    
DOI: 10.1021/ja9632825     Document Type: Article

References (65)

1. D, the kinetic isotope effect measured by comparing the rate of reaction with protonated substrate to that with deuterated substrate; and 1-D, 2-D, one-dimension, two-dimension, respectively.
2. The term "hydrogen transfer" is often used loosely to describe reactions involving hydrogen (atom), proton, or hydride particles, even though their chemical properties are remarkably different. Unless specifically mentioned, we will use the term "hydrogen" when referring to a particle that could be any one of the three - hydride, hydrogen atom, or proton.
3. Caldin, E.; Gold, V. Proton Transfer Reactions; Chapman and Hall: London, 1975.
4. Bell, R. P. The Tunnel Effect in Chemistry; Chapman and Hall: London, 1980.
5. Fain, B. Theory of Rate Processes in Condensed Media; Springer: Berlin, 1973.
6. Lefebvre, R. In Conceptual Trends in Quantum Chemistry; Calais, J. L., Kryachko, E., Eds.; Kluwer: Boston, in press; Vol. II.
7. Schowen, R. L. In Transition States of Biochemical Proesses; Gandour, R. D., Schowen, R. L., Eds.; Plenum: New York, 1978.
8. Jenks, W. P. Cold Spring Harbor Symp. Quant. Biol. 1987, 52, 65-73.
9. Cha, Y.; Murray, C. J.; Klinman, J. P. Science 1989, 243, 1325-1330.
10. Rucker, J.; Cha, Y.; Jonsson, T.; Grant, K. L.; Klinman, J. P. Biochemistry 1992, 31, 11489-11499.
11. Bahnson, B. J.; Park, D.-H.; Kim, K.; Plapp, B. V.; Klinman, J. P. Biochemistry 1993, 31, 5503-5507.
12. Alston, W. C.; Marianna, K.; Murray, C. J. Biochemistry 1996, 35, 12873-12881.
13. Grant, L. K.; Klinman, J. P. Biochemistry 1989, 28, 6957-6605.
14. Jonsson, T.; Edmondson, D. E.; Klinman, J. P. Biochemistry 1995,
15. Kohen, A.; Jonsson, T.; Klinman, J. Biochemistry In press.
16. Jonsson, T.; Glickman, M. H.; Sun, S. J.; Klinman, J. P. J. Am. Chem. Soc. 1996, 118, 10319-10320.
17. Rucker, J. B. Ph.D. Thesis, University of California, Berkeley, 1995.
18. Huskey, W. P. Phys. Org. Chem 1991, 4, 361-366.
19. Huskey, W. P.; Schowen, R. L. J. Am. Chem. Soc. 1983, 105, 5704-5706.
20. Bruno, W. J.; Bialek, W. Biophys. J. 1992, 63, 689-699.
21. Nelson, M. J.; Seitz, S. P. Curr. Opin. Struct. Biol. 1994, 4, 878-884.
22. Gardner, H. W. Biochim. Biophys. Acta 1991, 1084, 221-239.
23. Siedow, J. N. Annu. Rev. Plant Mol. Biol. 1991, 42, 145-188.
24. Glickman, M. H.; Klinman, J. P. Biochemistry 1995, 34, 14077-14092.
25. Glickman, M. H.; Wiseman, J.; Klinman, J. P. J. Am. Chem. Soc. 1994, 116, 793-794.
26. Glickman, M. H.; Klinman, J. P. Biochemistry 1996, 35, 12882-12892.
27. Bigeleisen, J.; Goepert-Mayer, M. J. Chem. Phys. 1947, 15, 261-267.
28. Bigeleisen, J. J. Chem. Phys. 1949, 17, 675-678.
29. Researchers within the isotope effect field often consider the Bigeleisen-Mayer equation to be a semiclassical theory (as opposed to fully quantum mechanical). In order to avoid confusion with the use of the term in quantum mechanics, e.g., the WKB approximation, we will not use the term in this fashion in this paper.
30. Stern, M. J.; Weston, R. E., Jr. J. Chem. Phys. 1974, 60, 2808-2814.
31. Dakhnovskii, Y.; Bursulaya, B.; Kim, H. J. J. Chem. Phys. 1995, 102, 7838-7849.
32. German, E. D.; Kuznetsov, A. M.; Dogonadze, R. R. J. Chem. Soc., Faraday Trans. 2 1980, 76, 1128-1146.
33. Bethe, H. A. In Handb. Phys.1933, 24/1, 452ff.
34. Lefebvre, R.; Moiseyev, N. J. Am. Chem. Soc. 1990, 112, 5052.
35. Rom, N.; Lefebvre, R.; Moiseyev, N. J. Chem. Phys. 1992, 95, 3562.
36. Rom, N.; Ryaboy, V.; Moiseyev, N. Chem. Phys. Lett. 1993, 204, 175.
37. deGroot, J. J. M. C.; Garssen, G. J.; Veldink, G. A.; Vliegenthart, J. F. G.; Boldingh, J. FEBS Lett. 1975, 56, 50-54.
38. Funk, M. O.; Carrol, R. T.; Sands, R. H.; Dunham, W. R. J. Am. Chem. Soc. 1990, 112, 5375-5376.
39. Schilstra, M. J.; Veldink, G. A.; Vliegenthart, J. F. G. Biochemistry 1994, 33, 3974-3979.
40. deGroot, J. J. M. C.; Garssen, G. J.; Vliegenthart, J. F. G.; Boldingh, J. Biochim. Biophys. Acta 1973, 326, 279-284.
41. Nelson, M. J.; Seitz, S. P.; Cowling, R. A. Biochemistry 1990, 29, 6897-6903.
42. Lomnitski, L.; Bar-Natan, R.; Sklan, D.; Grossman, S. Biochim. Biophys. Acta 1993, 1167, 331-338.
43. Maccarrone, M.; Veldink, G. A.; Vliegenthart, J. F. G.; Agro, A. F. Lipids 1995, 30, 51-54.
44. Nelson, M. J.; Cowling, R. A.; Seitz, S. P. Biochemistry 1994, 33, 4966-4973.
45. Wiseman, J. S. Biochemistry 1989, 28, 2106-2111.
46. deGroot, J. J. M. C.; Veldink, G. A.; Vliegenthart, J. F. G.; Boldingh, J.; Wever, R.; vanGelder, B. F. Biochim. Biophys. Acta 1975, 377, 71-79.
47. Chamulitrat, W.; Mason, R. P. J. Biol. Chem. 1989, 264, 20968-20973.
48. Lamb, W. E.; Retherford, R. C. Phys. Rev. 1950, 79, 599.
49. 1-(mD/mH)1/2 (e)
50. Wynne, K.; LeCours, S. M.; Galli, C.; Therien, M. J.; Hochstrasser, R. M. J. Am. Chem. Soc. 1995, 117, 3749-3753.
51. Johnston, H. S.; Rapp, D. J. Am. Chem. Soc. 1961, 83, 1.
52. Johnston, H. S.; Rapp, D. Adv. Chem. Phys. 1960, 3, 131.
53. Caldin, E. F. Chem. Rev. 1969, 69, 135-156.
54. Miller, W. H. Science 1986, 233, 171-177.
55. The area of a triangle is linearly proportional to its height, therefore for a symmetric 1-dimensional barrier the energy of activation would be proportional to an integration of the potential over the reaction pathway. In this case, the ratio of energies of activation for H and D would be given by the ratio of the respective integrated potentials, with other constants canceling out.
56. As a note, in the opposite scenario, whereby K(x) reaches a minimal value at x = 0 (i.e., a "loose transition state"), the height of the potential barrier (the "activation energy") is decreased compared to the one-dimensional model described above, and it is decreased to a greater extent for hydrogen than for deuterium. Since even the one-dimensional calculations produced isotope effects larger than the experimental results as seen in eq 7, this regime is obviously not the explanation for the isotope effects observed in the lipoxygenase reaction.
57. Feig, A. L.; Lippard, S. J. Chem. Rev. 1994, 94, 759-805.
58. Que, L. Struct. Bonding 1980, 40, 39-72.
59. Van der Heijdt, L. M.; Schilstra, M. J.; Feiters, M. C.; Nolting, H. F.; Hermes, C.; Veldink, G. A.; Vleiegenthart, J. F. J. Eur. J. Biochem. 1995, 231, 186-191.
60. Nelson, M. J. Biochemistry 1988, 27, 4273-4278.
61. Glickman, M. H. Ph.D. Dissertation Thesis, University of California, Berkeley, 1994.
62. Minor, W.; Steczko, J.; Stec, B.; Otwinowski, Z.; Bolin, J. T.; Walter, R.; Axelrod, B. Biochemistry 1996, 35, 10687-10701.
63. Scarrow, R. C.; Trimitsis, M. G.; Buck, C. P.; Grove, G. N.; Cowling, R. A.; Nelson, M. J. Biochemistry 1994, 33, 15023-15035.
64. He, G. X.; Arasaingham, R. D.; Zhang, G. H.; Bruice, T. C. J. Am. Chem. 1991, 113, 9828-9833.
65. Roecker, L.; Meyer, T. J. J. Am. Chem. Soc. 1987, 109, 746-754.