Exchange-enhanced reactivity in bond activation by metal-oxo enzymes and synthetic reagents

Nature Chemistry

Volumn 3, Issue 1, 2011, Pages 19-27

  Shaik, Sason ^a   Chen, Hui ^a   Janardanan, Deepa ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

DYES, REAGENTS, INDICATORS, MARKERS AND BUFFERS; ENZYME; METALLOPROTEIN; TRANSITION ELEMENT;

ARTICLE; CHEMISTRY; ELECTRON; INORGANIC CHEMISTRY; OXIDATION REDUCTION REACTION;

CHEMISTRY, BIOINORGANIC; ELECTRONS; ENZYMES; INDICATORS AND REAGENTS; METALLOPROTEINS; OXIDATION-REDUCTION; TRANSITION ELEMENTS;

EID: 78650366980     PISSN: 17554330     EISSN: 17554349     Source Type: Journal    
DOI: 10.1038/nchem.943     Document Type: Article

References (66)

1. Woodward, R. B. & Hoffmann, R. The Conservation of Orbital Symmetry (Verlag Chemie, 1970).
2. Fukui, K., Yonezawa, T. & Shingu, H. A molecular orbital theory of reactivity in aromatic hydrocarbons. J. Chem. Phys. 20, 722-725 (1952).
3. Shaik, S. & Hiberty, P. C. A Chemist's Guide to Valence Bond Theory (Wiley, 2008).
4. de Jong, G. T. & Bickelhaupt, F. M. Transition-state energy and position along the reaction coordinate in an extended activation strain model. ChemPhysChem 8, 1170-1181 (2007).
5. Hirao, H., Kumar, D., Thiel, W. & Shaik, S. Two states and two more in the mechanisms of hydroxylation and epoxidation by cytochrome P450. J. Am. Chem. Soc. 127, 13007-13018 (2005).
6. 2+: An oxidant more powerful than P450? J. Am. Chem. Soc. 127, 8026-8027 (2005).
7. Hirao, H., Kumar, D., Que, L. Jr & Shaik, S. Two-state reactivity in alkane hydroxylation by non-heme iron-oxo complexes. J. Am. Chem. Soc. 128, 8590-8606 (2006).
8. Shaik, S., Hirao, H. & Kumar, D. Reactivity of high-valent iron-oxo species in enzymes and synthetic reagents: A tale of many states. Acc. Chem. Res. 40, 532-542 (2007).
9. Janardanan, D., Wang, Y., Schyman, P., Que, L. Jr. & Shaik, S. The fundamental role of exchange-enhanced reactivity in C-H activation by S = 2 oxo iron (iv) complexes. Angew. Chem. Int. Ed. 49, 3342-3345 (2010).
10. de Visser, S. P. Propene activation by the oxo-iron active species of taurine/α-ketoglutarate dioxygenase (TauD) enzyme. How does the catalysis compare to heme-enzymes? J. Am. Chem. Soc. 128, 9813-9824 (2006).
11. 2+. J. Phys. Chem. C. 111, 12397-12406 (2007).
12. Bernasconi, L., Louwerse, M. J. & Baerends, E. J. The role of equatorial and axial ligands in promoting the activity of non-heme oxidoiron (iv) catalysts in alkane hydroxylation. Eur. J. Inorg. Chem. 3023-3033 (2007).
13. Wang, Y. & Han, K. Steric hindrance effect of the equatorial ligand on Fe (iv) O and Ru (iv) O complexes: a density functional study. J. Biol. Inorg. Chem. 351-359 (2010).
14. Ye, S. & Neese, F. Quantum chemical studies of C-H activation reactions by high-valent nonheme iron centers. Curr. Opin. Chem. Biol. 13, 89-98 (2009).
15. IV=O oxidants. Angew. Chem. Int. Ed. 47, 3356-3359 (2008).
16. Cho, K.-B., Shaik, S. & Nam, W. Theoretical predictions of a highly reactive non-heme Fe(IV)=O species with a high-spin ground state. Chem. Commun. 46, 4511-4513 (2010).
17. IV=O oxidants. Chem. Eur. J. 14, 1740-1756 (2008).
18. de Visser, S. P. What factors influence the ratio of C-H hydroxylation versus C=C epoxidation by a nonheme cytochrome P450 biomimetic? J. Am. Chem. Soc. 128, 15809-15818 (2006).
19. IV=O complexes: Fe-O bonding and its contributions to reactivity. J. Am. Chem. Soc. 129, 15983-15996 (2007).
20. Ortiz de Montellano, P. R. (ed.) Cytochrome P450: Structure, Mechanism, and Biochemistry 3rd edn (Kluwer Academic/Plenum, 2005).
21. Nam, W. High-valent iron (iv)-oxo complexes of heme and non-heme ligands in oxygenation reactions. Acc. Chem. Res. 40, 522-531 (2007).
22. Que, L. Jr The road to non-heme oxoferryls and beyond. Acc. Chem. Res. 40, 493-500 (2007).
23. Krebs, C., Fujimori, D. G., Walsh, C. T. & Bollinger, J. M. Jr Non-heme Fe(IV)-oxo intermediates. Acc. Chem. Res. 40, 484-492 (2007).
24. Sinnecker, S. et al. Spectroscopic and computational evaluation of the structure of the high-spin Fe(IV)-oxo intermediates in taurine: α-ketoglutarate dioxygenase from Escherichia coli and its His99Ala ligand variant. J. Am. Chem. Soc. 129, 6168-6179 (2007).
25. 2 activation pathways of non-heme iron oxygenases. Acc. Chem. Res. 40, 475-483 (2007).
26. Murray, L. J. & Lippard, S. J. Substrate trafficking and dioxygen activation in bacterial multicomponent monooxygesases. Acc. Chem. Res. 40, 466-474 (2007).
27. Neidig, M. L. et al. Spectroscopic and electronic structure studies of aromatic electrophilic attack and hydrogen-atom abstraction by non-heme iron enzymes. Proc. Natl Acad. Sci. USA 103, 12966-12973 (2006).
28. Bassan, A., Blomberg, M. R. A. & Siegbahn, P. E. M. Mechanism of dioxygen cleavage in tetrahydrobiopterin-dependent amino acid hydroxylases. Chem. Eur. J. 9, 106-115 (2003).
29. 2] diamond core for C-H bond cleavage. Nature Chem. 2, 400-405 (2010).
30. Schwarz, H. On the spin-forbiddeness of gas-phase ion-molecule reactions: A fruitful intersection of experimental and theoretical studies. Int. J. Mass. Spectrom. 237, 75-105 (2004).
31. Carter, E. A. & Goddard, W. A. III Relationships between bond energies in coordinatively unsaturated and coordinatively saturated transition-metal complexes: A quantitative guide for single, double, and triple bonds. J. Phys. Chem. 92, 5679-5683 (1988).
32. + through ZnH+. J. Phys. Chem. 91, 5616-5623 (1987).
33. +. J. Phys. Chem. 92, 2109-2115 (1988).
34. Filatov, M., Harris, N. & Shaik, S. A theoretical study of electronic factors affecting hydroxylation by model ferryl complexes of cytochrome P-450 and horseradish peroxidase. J. Chem. Soc. Perkin Trans. 2, 399-410 (1999).
35. Ballhausen, C. J. Quantum mechanics and chemical bonding in inorganic complexes. J. Chem. Educ. 56, 294-297 (1979).
36. Van Vleck, J. H. Valence strength and the magnetism of complex salts. J. Chem. Phys. 3, 807-813 (1935).
37. Goddard, W. A. III & Harding, L. B. The description of chemical bonding from ab initio calculations. Annu. Rev. Phys. Chem. 29, 363-396 (1978).
38. Cornehl, H. H., Heinemann, C., Schröder, D. & Schwarz, H. Gas-phase reactivity of lanthanide cations with hydrocarbons. Organometallics 14, 992-999 (1995).
39. Carroll, J. J. et al. Gas phase reactions of second-row transition metal atoms with small hydrocarbons: Experiment and theory. J. Phys. Chem. 99, 13955-13969 (1995).
40. 4F) with methane, ethane and propane. J. Am. Chem. Soc. 110, 411-423 (1988).
41. 2: The first example of cluster-mediated σ-bond activation by a transition metal center. J. Am. Chem. Soc. 116, 9710-9718 (1994).
42. cam and chloroperoxidase revealed from multireference ab initio QM/MM calculations. J. Chem. Theory Comput. 6, 940-953 (2010).
43. Chen, H., Lai, W. Z. & Shaik, S. Exchange-enhanced H-abstraction reactivity of high-valent non-heme iron (IV)-oxo from coupled cluster and density functional theories. J. Phys. Chem. Lett. 1, 1533-1540 (2010).
44. Shaik, S., Lai, W. Z., Chen, H. & Wang, Y. The valence bond way: Reactivity patterns of cytochrome P450 enzymes and synthetic analogs. Acc. Chem. Res. 43, 1154-1165 (2010).
45. 2+, M = V-Cu. Inorg. Chem. 48, 3628-3638 (2009).
46. Filatov, M. & Shaik, S. Theoretical investigation of two-state-reactivity pathways of H-H activation by FeO+: Addition-elimination, "rebound", and oxeneinsertion mechanisms. J. Phys. Chem. A 102, 3835-3846 (1998).
47. Schröder, D., Shaik, S. & Schwarz, H. Two-state reactivity as a new concept in organometallic chemistry. Acc. Chem. Res. 33, 139-145 (2000).
48. Shaik, S. et al. P450 enzymes: Their structure, reactivity, and selectivity-modeled by QM/MM calculations. Chem. Rev. 110, 949-1017 (2010).
49. Altun, A., Shaik, S. & Thiel, W. What is the active species of cytochrome P450 during camphor hydroxylation? QM/MM studies of different electronic states of compound I and of reduced and oxidized iron-oxo intermediates. J. Am. Chem. Soc. 129, 8978-8987 (2007).
50. Wang, D., Zhang, M., Bühlmann, P. & Que, L. Jr Redox potential and C-H bond cleaving properties of a nonheme Fe(IV)=O complex in aqueous solution. J. Am. Chem. Soc. 132, 7638-7644 (2010).
51. Latifi, R., Bagherzadeh, M. & de Visser, S. P. Origin of the correlation of the rate constant of substrate hydroxylation by nonheme iron (IV)-oxo complexes with the bond-dissociation energy of the C-H bond of the substrate. Chem. Eur. J. 15, 6651-6662 (2009).
52. Geng, C., Ye, S. & Neese, F. Analysis of reaction channels for alkane hydroxylation by nonheme iron (IV)-oxo complexes. Angew. Chem. Int. Ed. 49, 5717-5720 (2010).
53. Brandt, P., Norrby, P.-O., Daly, A. M. & Gilheany, D. G. Chromium-salenmediated alkene epoxidation: A theoretical and experimental study indicates the importance of spin-surface crossing and the presence of a discrete intermediate. Chem. Eur. J. 8, 4299-4307 (2002).
54. 2. J. Am. Chem. Soc. 124, 2454-2455 (2002).
55. Jin, N. & Groves, J. T. Unusual kinetic stability of a ground-state singlet oxomanganese (v) porphyrin. Evidence for a spin state crossing effect. J. Am. Chem. Soc. 121, 2923-2924 (1999).
56. De Angelis, F., Jin, N., Car, R. & Groves, J. T. Electronic structure and reactivity of isomeric oxo-Mn (v) porphyrins: Effects of spin-state crossing and pKa modulation. Inorg. Chem. 45, 4268-4276 (2006).
57. Balcells, D., Raynaud, C., Crabtree, R. H. & Eisenstein, O. The rebound mechanism in catalytic C-H oxidation by MnO (tpp) Cl from DFT studies: electronic nature of the active species. Chem. Commun. 744-746 (2008).
58. Khenkin, A. M., Kumar, D., Shaik, S. & Neumann, R. Characterization of manganese (V)-oxo polyoxometalate intermediates and their properties in oxygen-transfer reactions. J. Am. Chem. Soc. 128, 15451-15460 (2006).
59. Abashkin, Y. G., Collins, J. R. & Burt, S. K. (Salen) Mn(III)-catalyzed epoxidation reaction as a multichannel process with different spin states. Electronic tuning of asymmetric catalysis: A theoretical study. Inorg. Chem. 40, 4040-4048 (2001).
60. Balcells, D., Clot, E. & Eisenstein, O. C-H bond activation in transition metal species from a computational perspective. Chem. Rev. 110, 749-823 (2010).
61. Song, W. J. et al. Synthesis, characterization, and reactivities of manganese (V)-oxo porphyrin complexes. J. Am. Chem. Soc. 129, 1268-1277 (2007).
62. 2. J. Phys. Chem. 98, 6522-6529 (1994).
63. Poli, R. & Harvey, J. N. Spin-forbidden chemical reactions of transition metal compounds. New ideas and new computational techniques. Chem. Soc. Rev. 32, 1-8 (2003).
64. Shaik, S., Danovich, D., Schröder, D. & Schwarz, H. Two-state reactivity in organometallic gas-phase ion chemistry. Helv. Chim. Acta 78, 1393-1407 (1995).
65. Mayer, J. M. Hydrogen atom abstraction by metal-oxo complexes: Understanding the analogy with organic radical reactions. Acc. Chem. Res. 31, 441-450 (1998).
66. Sastri, C. V. et al. Axial ligand tuning of a nonheme iron (IV)-oxo unit for hydrogen atom abstraction. Proc. Natl Acad. Sci. USA 104, 19181-19186 (2007).