A compelling experimental test of the hypothesis that enzymes have evolved to enhance quantum mechanical tunneling in hydrogen transfer reactions: The β-neopentylcobalamin system combined with prior adocobalamin data

Inorganic Chemistry

Volumn 42, Issue 16, 2003, Pages 4849-4856

  Doll, Kenneth M ^a   Finke, Richard G ^a  

^a Veterinary Dentistry and Oral Surgery   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADOCOBALAMIN; BETA NEOPENTYLCOBALAMIN; COBALAMIN DERIVATIVE; COBAMAMIDE; ETHYLENE GLYCOL; HYDROGEN; METHYLMALONYL COENZYME A MUTASE; PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CATALYSIS; ENZYME ANALYSIS; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; PROTON TRANSPORT; QUANTUM MECHANICS; SYNTHESIS;

EID: 0042905762     PISSN: 00201669     EISSN: None     Source Type: Journal    
DOI: 10.1021/ic0300722     Document Type: Article

References (100)

1. Antoniou, D.; Schwartz, S. D. J. Phys. Chem. B 2001, 105, 5553.
2. Bahnson, B. J.; Klinman, J. P. Methods Enzymol. 1995, 249, 373.
3. Cha, Y.; Murray, C. J.; Klinman, J. P. Science 1989, 243, 1325.
4. Cha, Y.; Murray, C. J.; Klinman, J. P, Science 1989, 244, 244.
5. Chin, J. K.; Klinman, J. P. Biochemistry 2000, 39, 1278.
6. Grant, K. L.; Klinman, J. P. Biochemistry 1989, 28, 6597.
7. Kohen, A.; Klinman, J. P. Acc. Chem. Res. 1998, 31, 397.
8. Kohen, A.; Klinman, J. P. Chem. Biol. 1999, 6, R191.
9. Kohen, A.; Cannio, R.; Bartolucci, S.; Klinman. J. P. Nature 1999, 399, 496.
10. Kohen, A.; Klinman, J. P. J. Am. Chem. Soc. 2000, 122, 10738.
11. Miller, S. M.; Klinman, J. P. Biochemistry 1985, 24, 2114.
12. Northrop, D. B.; Cho, Y.-K. Biochemistry 2000, 39, 2406.
13. Rickert, K. W.; Klinman, J. P. Biochemistry 1999, 38, 12218.
14. Rucker, J.; Klinman, J. P. J. Am. Chem. Soc. 1999, 121, 1997.
15. Tsai, S.-C.; Klinman, J. P. Biochemistry 2001, 40, 2303.
16. Basran, J.; Sutcliffe, M. J.; Scrutton, N. S. Biochemistry 1999, 38, 3218.
17. Scrutton, N. S.; Basran, J.; Sutcliffe, M. J. Eur. J. Biochem. 1999, 264, 666.
18. Knapp, M. J.; Rickert, K.; Klinman, J. P. J. Am. Chem. Soc. 2002, 124, 3865.
19. Basran, J.; Sutcliffe, M. J.; Scrutton, N. S. J. Biol. Chem. 2001, 276, 24581.
20. Sutcliffe, M. J.; Scrutton, N. S. Trends Biochem. Sci. 2000, 25, 405.
21. Chowdhury, S.; Banerjee, R. J. Am. Chem. Soc. 2000, 122, 5417.
22. Dybala-Defratyka, A.; Paneth, P. J. Inorg. Biochem. 2001, 86, 681.
23. Alhambra, C.; Corchado, J. C.; Sanchez, M. L.; Gao, J.; Truhlar, D. G. J. Am. Chem. Soc. 2000, 122, 8197.
24. Alhambra, C.; Luz Sanchez, M.; Corchado, J.; Gao, J.; Truhlar, D. G. Chem. Phys. Lett. 2001, 347, 512.
25. Villa, J.; Strajbl, M.; Glennon, T. M.; Sham, Y. Y.; Chu, Z. T.; Warshel, A. Proc. Natl. Acad. Sci. U.S.A. 2000, 97, 11899.
26. Villa, J.; Warshel, A. J. Phys. Chem. B 2001, 105, 7887.
27. Shurki, A.; Strajbl, M.; Villa, J.; Warshel, A. J. Am. Chem. Soc. 2002, 124, 4097.
28. Cui, Q.; Karplus, M. J. Am. Chem. Soc. 2002, 124, 3093.
29. Shibata, N.; Masuda, J.; Tobimatsu, T.; Toraya, T.; Suto, K.; Morimoto, Y.; Yasuoka, N. Structure 1999, 7, 997.
30. McGee, D. E. Diol dehydratase: purification, structural characterization, and mechanism of action. Ph.D. Thesis, California Institute of Technology, 1983.
31. Toraya, T. Cell. Mol. Life Sci. 2000, 57, 106.
32. Toraya, T. J. Mol. Catal. B: Enzymol. 2000, 10, 87.
33. Bandarian, V.; Reed, G. H. Biochemistry 2000, 39, 12069.
34. Babior, B. M.; Weisblat, D. A. J. Biol. Chem. 1971, 246, 6064.
35. Bruice, T. C.; Benkovic, S. J. Biochemistry 2000, 39, 6267.
36. Northrop, D. B. Methods (San Diego, CA, U.S.) 2001, 24, 117.
37. Basran, J.; Patel, S.; Sutcliffe, M. J.; Scrutton, N. S. J. Biol. Chem. 2001, 276, 6234.
38. Peticolas, W. L. Methods Enzymol. 1979, 61, 425.
39. Debrunner, P. G.; Frauenfelder, H. Annu. Rev. Phys. Chem. 1982, 33, 283.
40. Go, N.; Noguti, T.; Nishikawa, T. Proc. Natl. Acad. Sci. U.S.A. 1983, 80, 3696.
41. Frauenfelder, H.; Wolynes, P. G. Science 1985, 229, 337.
42. Noguti, T.; Go, N. Proteins: Struct., Funct., Genet. 1989, 5, 104.
43. Genberg, L.; Richard, L.; McLendon, G.; Miller, R. J. D. Science 1991, 251, 1051.
44. Garr, C. D.; Finke, R. G. Inorg. Chem. 1993, 32, 4414.
45. Tarek, M.; Martyna, G. J.; Tobias, D. J. J. Am. Chem. Soc. 2000. 122, 10450.
46. Tama, F.; Miyashita, O.; Kitao, A.; Go, N. Eur. Biophys. J. 2000, 29, 472.
47. Tama, F.; Gadea, F. X.; Marques, O.; Sanejouand, Y.-H. Proteins: Struct., Funct., Genet. 2000, 41, 1.
48. Kim, Y.; Kreevoy, M. M. J. Am. Chem. Soc. 1992, 114, 7116.
49. Kwart, H. Acc. Chem. Res. 1982, 15, 401.
50. Chih, H.-W.; Marsh, E. N. G. Biochemistry 2001, 40, 13060.
51. Marsh, E. N. G. Essays Biochem. 1999, 34, 139.
52. Marsh, E. N. G.; Ballou, D. P. Biochemistry, 1998, 37, 11864.
53. Huhta, M. S.; Ciceri, D.; Golding, B. T.; Marsh, E. N. G. Biochemistry 2002, 41, 3200.
54. Abeles, R. H.; Essenberg, M. K.; Frey, P. A. J. Am. Chem. Soc. 1971, 93, 1242.
55. 28group finds that there is no significant tunneling enhancement in the triosephosphate isomerase system when gas, solution, or enzyme systems are simulated. This is one reason an experimental test such as the present work was needed and, hence, undertaken.
56. Doll, K. M.; Bender, B. R.; Finke, R. G. J. Am. Chem. Soc. 2003, in press.
57. 5960Convincing experimental support for the validity of comparing these H· abstractions is found in the fact that all three enzyme-free systems studied, NpCbl, AdoCbl, and 8-MeOCbl, give results identical within experimental error to the AdoCbl-dependent methylmalonyl-CoA mutase system; that is, the results themselves strongly support, ex post facto, the comparison of the slightly different enzyme-based and enzyme-free solution systems.
58. Karelson, M.; Katritzky, A. R.; Zerner, M. C. J. Org. Chem. 1991, 56, 134.
59. Berkowitz, J.; Ellison, G. B.; Gutman, D. J. Phys. Chem. 1994, 98, 2744.
60. CRC Handbook of Chemistry and Physics, 81st ed.; Lide, D. R., Ed.; CRC Press: Boca Raton, FL, 2000, p G-64.
61. Bell, R. P. The Tunnel Effect in Chemistry; Chapman and Hall: New York, 1980.
62. Berger, U.; Kolliker, S.; Oehme, M. Chimia 1999, 53, 492.
63. Siethoff, C.; Wagner-Redeker, W.; Schafer, M.; Linscheid, M. Chimia 1999, 53, 484.
64. 12. Ph.D. Thesis, University of Oregon, Chemistry, 1986.
65. Duong, K. N. V.; Gaudemer, A.; Johnson, M. O.; Quillivic, R.; Zylber, J. Tetrahedron Lett. 1975, 2997.
66. Zylber, J.; Pontikis, R.; Merrien, A.; Merienne, C.; Baran-Marszak, M.; Gaudemer, A. Tetrahedron 1980, 36, 1579.
67. Waddington, M. D.; Finke, R. G. J. Am. Chem. Soc. 1993, 115, 4629.
68. Brown, K. L., Peck, S. In Organometallic Synthesis; King, R. B.; Eisch, J. J., Ed.; Elsevier: New York, 1988; Vol. 4, p 304-315.
69. Brown, K. L.; Evans, D. R. Inorg. Chem. 1994, 33, 6380.
70. Brown, K. L.; Brooks, H. B. Inorg. Chem. 1991, 30, 3420.
71. Grate, J. H.; Schrauzer, G. N. J. Am. Chem. Soc. 1979, 101, 4601.
72. 5 times more reactive than Np-I in nucleophilic displacement reactions.
73. Streitweiser, A. J. Solvolytic Displacement Reactions; McGraw-Hill Book Company: New York, 1962.
74. Lowry, T. H.; Richardson, K. S. Mechanism and Theory in Organic Chemistry, 3rd ed.; Harper and Row, New York, 1987.
75. Zou, X.; Brown, K. L. J. Am. Chem. Soc. 1993, 115, 6689.
76. Brown, K. L.; Zou, X. Inorg. Chem. 1992, 31, 2541.
77. Brown, K. L.; Zou, X. Inorg. Chem. 1991, 30, 4185.
78. Hay, B. P.; Finke, R. G. J. Am. Chem. Soc. 1987, 109, 8012.
79. Schrauzer, G. N.; Grate, J. H. J. Am. Chem. Soc. 1981, 103, 541.
80. Kim, S. H.; Chen, H. L.; Feilchenfeld, N.: Halpern, J. J. Am. Chem. Soc. 1988, 110, 3120.
81. We attempted to measure the molecular ions directly by lowering the energy of the electron impact filament, but were not successful as expected since ionized, unfragmented neopentane+ is notoriously difficult to detect.
82. Silverstein, R. M.; Bassler, G. C.; Morrill, T. C. Spectrometric Identification of Organic Compounds, 4th ed.; Wiley and Sons: New York, 1981.
83. Frei, H.; Ha, T.-K.; Meyer, R.: Guenthard, H. H. Chem. Phys. 1977, 25, 271.
84. The H· (or D·) abstraction from the C-H and not the O-H(D) is as expected from Ingold and co-worker's literature: they demonstrated that the abstraction reaction of hydrogen from MeOH and MeOD by methyl radical proceeds at the same rate at 77 K, that is, that C-H abstraction is occurring.
85. Doba, T.; Ingold, K. U.; Siebrand, W.; Wildman, T. A. Faraday Discuss. Chem. Soc. 1984, 78, 175.
86. Brunton, G.; Griller, D.; Barclay, L. R. C.; Ingold, K. U. J. Am. Chem. Soc. 1976, 98, 6803. This is a classic piece of work that anyone interested in H tunneling will wish to read.
87. Siebrand, W.; Wildman, T. A.; Zgierski, J. Am. Chem. Soc. 1984, 106, 4083.
88. Siebrand, W.; Wildman, T. A.; Zgierski, J. Am. Chem. Soc. 1984, 106, 4089.
89. Doba, T.; Ingold, K. U.; Lusztyk, J.; Siebrand, W.; Wildman, T. A. J. Chem. Phys. 1993, 98. 2962.
90. (a) Smedarchina, Z.; Siebrand, W.; Fernández-Ramos, A.; Cui, Q. J. Am. Chem. Soc. 2003, 125, 243. This valuable paper also makes it rather clear that only the proper quantum mechanical treatment of KIEs, and not GS-ZPE corrected transition-state theory, can yield reliable KIEs for comparison to experiment. (b) Siebrand, W., Doll, K. M., Finke, R. G. manuscript in preparation.
91. (a) Smedarchina, Z.; Siebrand, W.; Fernández-Ramos, A.; Cui, Q. J. Am. Chem. Soc. 2003, 125, 243. This valuable paper also makes it rather clear that only the proper quantum mechanical treatment of KIEs, and not GS-ZPE corrected transition-state theory, can yield reliable KIEs for comparison to experiment. (b) Siebrand, W., Doll, K. M., Finke, R. G. manuscript in preparation.
92. Bachovchin, W. W.; Eagar, R. G., Jr.; Moore, K. W.; Richards, J. H. Biochemistry 1977, 16, 1082.
93. Bachovchin, W. W.; Moore, K. W.; Richards, J. H. Biochemistry 1978, 17, 2218.
94. +-transfer distance and increasing the tunneling mode anharmonicity, the two most important parameters in their tunneling model.
95. (b) Private communication from Dr. Siebrand.
96. Knapp, M. J.; Rickert, K. W.; Klinman, J. P. J. Am. Chem. Soc. 2002, 124, 3865. Siebrand and Smedarchina show that there is no statistically valid difference in the data in this paper for mutant vs wild-type enzyme (due to the too narrow temperature range over which the data could be obtained), thereby negating the claimed support in this paper for the putative protein-squeezing mechanism.
97. Hay, B, P.; Finke, R. G. Polyhedron 1988, 7. 1469.
98. Landauer, S. R.; Rydon, H. N. J. Chem. Soc. 1953, 2224.
99. Roberts, D. D.; Snyder, R. C., Jr. J. Org. Chem. 1980, 45, 4052.
100. Tipson, R. S. J. Org. Chem. 1944, 9, 235.