Two-state reactivity in the rebound step of alkane hydroxylation by cytochrome P-450: Origins of free radicals with finite lifetimes

Angewandte Chemie - International Edition

Volumn 39, Issue 11, 2000, Pages 2003-2007

  Harris, Nathan ^a   Cohen, Shimrit ^a   Filatov, Michael ^a   Ogliaro, François ^a   Shaik, Sason ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

Density functional calculations center dot enzyme catalysis; Hydroxylations; Oxygenases; Radicals

Indexed keywords

ALKANE; CYTOCHROME P450; FREE RADICAL;

ARTICLE; ELECTRON TRANSPORT; FINITE ELEMENT ANALYSIS; GEOMETRY; HYDROXYLATION; REACTION ANALYSIS;

EID: 0034595865     PISSN: 14337851     EISSN: None     Source Type: Journal    
DOI: 10.1002/1521-3773(20000602)39:11<2003::AID-ANIE2003>3.0.CO;2-M     Document Type: Article

References (35)

1. M. Sono, M. P. Roach, E. D. Coulter, J. H. Dawson, Chem. Rev. 1996, 96, 2841.
2. a) J. T. Groves, J. Chem. Educ. 1985, 62, 928;
3. b) J. T. Groves, G. A. McClusky, J. Am. Chem. Soc. 1976, 98, 859.
4. a) J. T. Groves, Y.-Z. Hang in Cytochrome P450: Structure, Mechanisms and Biochemistry, 2nd ed. (Ed.: P.R. Ortiz de Montellano), Plenum, New York, 1995, chap. 1;
5. b) B. Meunier, Chem. Rev. 1992, 92, 1411;
6. c) W. D. Woggon, Top. Curr. Chem. 1996, 184, 40.
7. a) J. I. Manchester, J. P. Dinnocenzo, L. A. Higgins, J. P. Jones, J. Am. Chem. Soc. 1997, 119, 5069;
8. b) The dimethyl aniline substrates in ref. [4a] were suggested later to undergo an initial electron transfer by the ferryl-oxene species of horseradish peroxidase and by a synthetic ferryl-oxene model (Y. Goto, Y. Watanabe, S. Fukuzumi, J. P. Jones, J. P. Dinnocenzo, J. Am. Chem. Soc. 1998, 120, 10762). This conclusion does not, however, pertain to the toluene, p-xylene, and benzyl alcohol species in ref. [4a]. Furthermore, all the model ferryl-oxene systems, used in the study, are better electron acceptors than the cytochrome P-450 ferryl-oxene complex so that the results may not pertain at all to oxidation by cytochrome P-450.
9. a) M. Newcomb, M.-H. Le Tadic, D. A. Putt, P. F. Hollenberg, J. Am. Chem. Soc. 1995, 117, 3312;
10. b) M. Newcomb, M.-H. Le Tadic-Beadatti, D. L. Chestney, E. S. Roberts, P. F. Hollenberg, J. Am. Chem. Soc. 1995, 117, 12085;
11. c) P. H. Toy, M. Newcomb, P. F. Hollenberg, J. Am. Chem. Soc. 1998, 120, 7719.
12. IIIOH] (S = 1) the ground state. This is in accord with electrochemical results in: J. T. Groves, Z. Gross, M. K. Stern, Inorg. Chem. 1994, 33, 5065
13. IIIOH] (S = 1) the ground state. This is in accord with electrochemical results in: J. T. Groves, Z. Gross, M. K. Stern, Inorg. Chem. 1994, 33, 5065
14. IIIOH] (S = 1) the ground state. This is in accord with electrochemical results in: J. T. Groves, Z. Gross, M. K. Stern, Inorg. Chem. 1994, 33, 5065
15. 3S model.
16. S. Shaik, M. Filatov, D. Schroder, H. Schwarz, Chem. Eur. J. 1998, 4, 193.
17. P. J. Stevens, F. J. Devlin, C. F. Chablowski, M. J. Frisch, J. Phys. Chem. 1994, 98, 11623.
18. JAGUAR 3.5, Schrodinger, Inc., Portland, OR. 1998. The program employs the restricted open-shell B3LYP method.
19. GAUSSIAN98, Gaussian, Inc., Pittsburgh, PA, 1998.
20. J. P. Hay, W. R. Wadt, J. Chem. Phys. 1985, 82, 299.
21. a) The state with maximum spin (S = 5/2) did not converge in our calculations. However, it must be kept in mind that whether the ground state of the product ferric-alcohol complex is S = 5/2 or S = 1/2 does not have bearing on the conclusions of this study, as summarized in Figure 2. What matters is the behavior of states obtained by the two spin coupling modes in Scheme 2.
22. b) Density functional calculations of corresponding ferric - water complexes give S = 1/2 ground state and a higher energy S = 5/2 state. See: M. Filatov, N. Harris, S. Shaik, J. Chem. Soc. Perkin Trans. 2 1999, 399; M. T. Green, J. Am. Chem. Soc. 1998, 120, 10772. This is supported by experimental assignment. See: H. Thomann, M. Bernardo, D. Goldfrab, P. M. H. Kroneck, V. Ulrich, J. Am. Chem. Soc. 1995, 117, 8243. However, a recent experimental investigation of a model compound with a spatially fixed thiophenoxy ligand shows an S = 5/2 ground state and indicates the role of the protein in stabilizing the S = 1/2 ground state, as predicted initially by Harris and Loew. See: H. Aissaoui, R. Bachmann, A. Schweiger, W.-D. Woggon, Angew. Chem. 1998, 110, 3191; Angew. Chem. Int. Ed. 1998, 37, 2998; D. Harris, G. H. Loew, J. Am. Chem. Soc. 1993, 115, 8775.
23. b) Density functional calculations of corresponding ferric - water complexes give S = 1/2 ground state and a higher energy S = 5/2 state. See: M. Filatov, N. Harris, S. Shaik, J. Chem. Soc. Perkin Trans. 2 1999, 399; M. T. Green, J. Am. Chem. Soc. 1998, 120, 10772. This is supported by experimental assignment. See: H. Thomann, M. Bernardo, D. Goldfrab, P. M. H. Kroneck, V. Ulrich, J. Am. Chem. Soc. 1995, 117, 8243. However, a recent experimental investigation of a model compound with a spatially fixed thiophenoxy ligand shows an S = 5/2 ground state and indicates the role of the protein in stabilizing the S = 1/2 ground state, as predicted initially by Harris and Loew. See: H. Aissaoui, R. Bachmann, A. Schweiger, W.-D. Woggon, Angew. Chem. 1998, 110, 3191; Angew. Chem. Int. Ed. 1998, 37, 2998; D. Harris, G. H. Loew, J. Am. Chem. Soc. 1993, 115, 8775.
24. b) Density functional calculations of corresponding ferric - water complexes give S = 1/2 ground state and a higher energy S = 5/2 state. See: M. Filatov, N. Harris, S. Shaik, J. Chem. Soc. Perkin Trans. 2 1999, 399; M. T. Green, J. Am. Chem. Soc. 1998, 120, 10772. This is supported by experimental assignment. See: H. Thomann, M. Bernardo, D. Goldfrab, P. M. H. Kroneck, V. Ulrich, J. Am. Chem. Soc. 1995, 117, 8243. However, a recent experimental investigation of a model compound with a spatially fixed thiophenoxy ligand shows an S = 5/2 ground state and indicates the role of the protein in stabilizing the S = 1/2 ground state, as predicted initially by Harris and Loew. See: H. Aissaoui, R. Bachmann, A. Schweiger, W.-D. Woggon, Angew. Chem. 1998, 110, 3191; Angew. Chem. Int. Ed. 1998, 37, 2998; D. Harris, G. H. Loew, J. Am. Chem. Soc. 1993, 115, 8775.
25. b) Density functional calculations of corresponding ferric - water complexes give S = 1/2 ground state and a higher energy S = 5/2 state. See: M. Filatov, N. Harris, S. Shaik, J. Chem. Soc. Perkin Trans. 2 1999, 399; M. T. Green, J. Am. Chem. Soc. 1998, 120, 10772. This is supported by experimental assignment. See: H. Thomann, M. Bernardo, D. Goldfrab, P. M. H. Kroneck, V. Ulrich, J. Am. Chem. Soc. 1995, 117, 8243. However, a recent experimental investigation of a model compound with a spatially fixed thiophenoxy ligand shows an S = 5/2 ground state and indicates the role of the protein in stabilizing the S = 1/2 ground state, as predicted initially by Harris and Loew. See: H. Aissaoui, R. Bachmann, A. Schweiger, W.-D. Woggon, Angew. Chem. 1998, 110, 3191; Angew. Chem. Int. Ed. 1998, 37, 2998; D. Harris, G. H. Loew, J. Am. Chem. Soc. 1993, 115, 8775.
26. b) Density functional calculations of corresponding ferric - water complexes give S = 1/2 ground state and a higher energy S = 5/2 state. See: M. Filatov, N. Harris, S. Shaik, J. Chem. Soc. Perkin Trans. 2 1999, 399; M. T. Green, J. Am. Chem. Soc. 1998, 120, 10772. This is supported by experimental assignment. See: H. Thomann, M. Bernardo, D. Goldfrab, P. M. H. Kroneck, V. Ulrich, J. Am. Chem. Soc. 1995, 117, 8243. However, a recent experimental investigation of a model compound with a spatially fixed thiophenoxy ligand shows an S = 5/2 ground state and indicates the role of the protein in stabilizing the S = 1/2 ground state, as predicted initially by Harris and Loew. See: H. Aissaoui, R. Bachmann, A. Schweiger, W.-D. Woggon, Angew. Chem. 1998, 110, 3191; Angew. Chem. Int. Ed. 1998, 37, 2998; D. Harris, G. H. Loew, J. Am. Chem. Soc. 1993, 115, 8775.
27. b) Density functional calculations of corresponding ferric - water complexes give S = 1/2 ground state and a higher energy S = 5/2 state. See: M. Filatov, N. Harris, S. Shaik, J. Chem. Soc. Perkin Trans. 2 1999, 399; M. T. Green, J. Am. Chem. Soc. 1998, 120, 10772. This is supported by experimental assignment. See: H. Thomann, M. Bernardo, D. Goldfrab, P. M. H. Kroneck, V. Ulrich, J. Am. Chem. Soc. 1995, 117, 8243. However, a recent experimental investigation of a model compound with a spatially fixed thiophenoxy ligand shows an S = 5/2 ground state and indicates the role of the protein in stabilizing the S = 1/2 ground state, as predicted initially by Harris and Loew. See: H. Aissaoui, R. Bachmann, A. Schweiger, W.-D. Woggon, Angew. Chem. 1998, 110, 3191; Angew. Chem. Int. Ed. 1998, 37, 2998; D. Harris, G. H. Loew, J. Am. Chem. Soc. 1993, 115, 8775.
28. H. Li, S. Narashmhulu, L. M. Havran, J. D. Winkler, T. L. Poulos, J. Am. Chem. Soc. 1995, 117, 6297.
29. A direct OH transfer mechanism would entail spin-state crossing to the S = 5/2 state of the five-coordinate ferric complex (for example, see: ref. [1]).
30. All HS data are obtained with B3LYP using JAGUAR 3.5 (ref. [9]). The LS profile is calculated with the unrestricted B3LYP method in GAUSSIAN 98 (ref. [10]). For convenience, the zero of the energy scale in Figure 2 is common to the LS and HS curves.
31. a) M. Filatov, W. Thiel, Chem. Phys. Lett. 1998, 295, 467;
32. b) H. Basch, S. Hoz, J. Phys. Chem. A 1997, 101, 4416;
33. c) S. Skokov, R. A. Wheeler, Chem. Phys. Lett. 1997, 271, 251;
34. 1 relative to the CASPT2 result which seems to overestimate the barrier.[17]
35. M. Filatov, S. Shaik, J. Phys. Chem. A 1998, 102, 3835.