Substrate hydroxylation in methane monooxygenase: Quantitative modeling via mixed quantum mechanics/molecular mechanics techniques

Journal of the American Chemical Society

Volumn 127, Issue 3, 2005, Pages 1025-1037

  Gherman, Benjamin F ^a   Lippard, Stephen J ^b   Friesner, Richard A ^a  

^a Och Spine at New York Presbyterian Hospitals   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CATALYSIS; ELECTROSTATICS; ENTROPY; FREE ENERGY; ISOTOPES; PROBABILITY DENSITY FUNCTION; PROTEINS; QUANTUM THEORY; SUBSTRATES; VAN DER WAALS FORCES;

KINETIC ISOTOPE EFFECT (KIE); MOLECULAR MECHANICS (MM); SUBSTRATE HYDROXYLATION;

METHANE;

ACETONITRILE; ETHANE; FLUOROMETHANE; ISOTOPE; METHANE; METHANE MONOOXYGENASE; METHANE MONOOXYGENASE HYDROXYLASE; METHANOL; NITROMETHANE; UNCLASSIFIED DRUG;

ACCURACY; ARTICLE; CATALYSIS; CHEMICAL REACTION KINETICS; DENSITY FUNCTIONAL THEORY; ELECTRICITY; ENERGY; ENTROPY; ENZYME SUBSTRATE COMPLEX; HYDROXYLATION; KINETIC ISOTOPE EFFECT; MECHANICAL STRESS; MICHAELIS MENTEN KINETICS; MODEL; MOLECULAR INTERACTION; MOLECULAR MECHANICS; QUANTUM MECHANICS;

ACETONITRILES; CATALYSIS; ETHANE; HYDROPHOBICITY; HYDROXYLATION; KINETICS; METHANE; METHANOL; MODELS, MOLECULAR; OXYGENASES; QUANTUM THEORY; THERMODYNAMICS;

EID: 12444307479     PISSN: 00027863     EISSN: None     Source Type: Journal    
DOI: 10.1021/ja049847b     Document Type: Article

References (90)

1. Hanson, R. S.; Hanson, T. E. Microbiol. Rev. 1996, 60, 439-471.
2. Lipscomb, J. D. Annu. Rev. Microbiol. 1994, 48, 371-399.
3. Liu, K. E.; Lippard, S. J. Adv. Inorg. Chem. 1995, 42, 263-289.
4. Feig, A. L.; Lippard, S. J. Chem. Rev. 1994, 94, 759-805.
5. Wallar, B. J.; Lipscomb, J. D. Chem. Rev. 1996, 96, 2625-2657.
6. Merkx, M.; Kopp, D. A.; Sazinsky, M. H.; Blazyk, J. L.; Müller, J.; Lippard, S. J. Angew. Chem., Int. Ed. 2001, 40, 2782-2807.
7. Baik, M.-H.; Newcomb, M.; Friesner, R. A.; Lippard, S. J. Chem. Rev. 2003, 103, 2385-2420.
8. Gherman, B. F.; Baik, M.-H.; Lippard, S. J.; Friesner, R. A. J. Am. Chem. Soc. 2004, 126, 2978-2990.
9. Rosenzweig, A. C.; Frederick, C. A.; Lippard, S. J.; Nordlund, P. Nature 1993, 366, 537-543.
10. Rosenzweig, A. C.; Nordlund, P.; Takahara, P. M.; Frederick, C. A.; Lippard, S. J. Chem. Biol. 1995, 2, 409-418.
11. Whillington, D. A.; Lippard, S. J. J. Am. Chem. Soc. 2001, 123, 827-838.
12. Guallar, V.; Gherman, B. F.; Lippard, S. J.; Friesner, R. A. Curr. Opin. Chem. Biol. 2002, 6, 236-242.
13. Guallar, V.; Baik, M.-H.; Lippard, S. J.; Friesner, R. A. Proc. Natl. Acad. Sci. U.S.A. 2003, 100, 6998-7002.
14. Wirstam, M.; Lippard, S. J.; Friesner, R. A. J. Am. Chem. Soc. 2003, 125, 3980-3987.
15. Philipp, D. M.; Friesner, R. A. J. Comput. Chem. 1999, 20, 1468-1494.
16. Murphy, R. B.; Philipp, D. M.; Friesner, R. A. J. Comput. Chem. 2000, 21, 1442-1457.
17. Murphy, R. B.; Philipp, D. M.; Friesner, R. A. Chem. Phys. Lett. 2000, 321, 113-120.
18. Qsite; Schrödinger, Inc.: Portland, OR, 2000.
19. Ambundo, E. A.; Friesner, R. A.; Lippard, S. J. J. Am. Chem. Soc. 2002, 124, 8770-8771.
20. Liu, K. E.; Wang, D. L.; Huynh, B. H.; Edmondson, D. E.; Salifoglou, A.; Lippard, S. J. J. Am. Chem. Soc. 1994, 116, 7465-7466.
21. Lee, S. K.; Nesheim, J. C.; Lipscomb, J. D. J. Biol. Chem. 1993, 265, 21569-21577.
22. Brazeau, B. J.; Lipscomb, J. D. Biochemistry 2000, 39, 13503-13515.
23. Liu, K. E.; Valentine, A. M.; Wang, D. L.; Huynh, B. H.; Edmondson, D. E.; Salifoglou, A.; Lippard, S. J. J. Am. Chem. Soc. 1995, 117, 10174-10185.
24. Shu, L. J.; Nesheim, J. C.; Kauffmann, K.; Münck, E.; Lipscomb, J. D.; Que, L. Science 1997, 275, 515-518.
25. Lee, S. K.; Fox, B. G.; Froland, W. A.; Lipscomb, J. D.; Münck, E. J. Am. Chem. Soc. 1993, 115, 6450-6451.
26. Nesheim, J. C.; Lipscomb, J. D. Biochemistry 1996, 35, 10240-10247.
27. Valentine, A. M.; Stahl, S. S.; Lippard, S. J. J. Am. Chem. Soc. 1999, 121, 3876-3887.
28. Gherman, B. F.; Dunietz, B. D.; Whittington, D. A.; Lippard, S. J.; Friesner, R. A. J. Am. Chem. Soc. 2001, 123, 3836-3837.
29. Brazeau, B. J.; Wallar, B. J.; Lipscomb, J. D. J. Am. Chem. Soc. 2001, 123, 10421-10422.
30. Muthusamy, M.; Ambundo, E. A.; George, S. J.; Lippard, S. J.; Thorneley, R. N. F. J. Am. Chem. Soc. 2003, 125, 11150-11151.
31. Wallar, B. J.; Lipscomb, J. D. Biochemistry 2001, 40, 2220-2233.
32. Brazeau, B. J.; Lipscomb, J. D. Biochemistry 2003, 42, 5618-5631.
33. Siegbahn, P. E. M. Inorg. Chem. 1999, 38, 2880-2889.
34. Siegbahn, P. E. M. J. Biol. Inorg. Chem. 2001, 6, 27-45.
35. Basch, H.; Mogi, K.; Musaev, D. G.; Morokuma, K. J. Am. Chem. Soc. 1999, 121, 7249-7256.
36. Basch, H.; Musaev, D. G.; Mogi, K.; Morokuma, K. J. Phys. Chem. A 2001, 105, 3615-3622.
37. Yoshizawa, K.; Ohta, T.; Yamabe, T.; Hoffmann, R. J. Am. Chem. Soc. 1997, 119, 12311-12321.
38. Yoshizawa, K.; Yamabe, T.; Hoffmann, R. New J. Chem. 1997, 21, 151-161.
39. Yoshizawa, K.; Ohta, T.; Yamabe, T. Bull. Chem. Soc. Jpn. 1998, 71, 1899-1909.
40. Yoshizawa, K.; Suzuki, A.; Shiota, Y.; Yamabe, T. Bull. Chem. Soc. Jpn. 2000, 73, 815-827.
41. Yoshizawa, K. J. Inorg. Biochem. 2000, 78, 23-34.
42. Yoshizawa, K. Coord. Chem. Rev. 2002, 226, 251-259.
43. Torrent, M.; Vreven, T.; Musaev, D. G.; Morokuma, K.; Farkas, O.; Schlegel, H. B. J. Am. Chem. Soc. 2002, 124, 192-193.
44. Johnson, B. G.; Gill, P. M. W.; Pople, J. A. J. Chem. Phys. 1993, 98, 5612-5626.
45. Lee, C. T.; Yang, W. T.; Parr, R. G. Phys. Rev. B 1988, 37, 785-789.
46. Becke, A. D. J. Chem. Phys. 1993, 98, 1372-1377.
47. Becke, A. D. J. Chem. Phys. 1993, 98, 5648-5652.
48. Curtiss, L. A.; Raghavachari, K.; Redfern, P. C.; Pople, J. A. J. Chem. Phys. 1997, 106, 1063-1079.
49. Bauschlicher, C. W. Chem. Phys. Lett. 1995, 246, 40-44.
50. Ricca, A.; Bauschlicher, C. W. Theor. Chim. Acta 1995, 92, 123-131.
51. Ricca, A.; Bauschlicher, C. W. J. Phys. Chem. 1995, 99, 5922-5926.
52. Ricca, A.; Bauschlicher, C. W. J. Phys. Chem. A 1997, 101, 8949-8955.
53. Glukhovtsev, M. N.; Bach, R. D.; Nagel, C. J. J. Phys. Chem. A 1997, 101, 316-323.
54. Blomberg, M. R. A.; Siegbahn, P. E. M.; Svensson, M. J. Chem. Phys. 1996, 104, 9546-9554.
55. Hascall, T.; Baik, M. H.; Bridgewater, B. A.; Shin, J. H.; Churchill, D. G.; Friesner, R. A.; Parkin, G. Chem. Commun. 2002, 2644-2645.
56. Shin, J. H.; Bridgewater, B. M.; Churchill, D. G.; Baik, M. H.; Friesner, R. A.; Parkin, G. J. Am. Chem. Soc. 2001, 123, 10111-10112.
57. Bergquist, C.; Storrie, H.; Koutcher, L.; Bridgewater, B. M.; Friesner, R. A.; Parkin, G. J. Am. Chem. Soc. 2000, 122, 12651-12658.
58. Bridgewater, B. M.; Fillebeen, T.; Friesner, R. A.; Parkin, G. J. Chem. Soc., Dalton Trans. 2000, 4494-4496.
59. Bergquist, C.; Bridgewater, B. M.; Harlan, C. J.; Norton, J. R.; Friesner, R. A.; Parkin, G. J. Am. Chem. Soc. 2000, 122, 10581-10590.
60. Hascall, T.; Rabinovich, D.; Murphy, V. J.; Beachy, M. D.; Friesner, R. A.; Parkin, G. J. Am. Chem. Soc. 1999, 121, 11402-11417.
61. Baik, M. H.; Lee, D.; Friesner, R. A.; Lippard, S. J. Isr. J. Chem. 2001, 41, 173-186.
62. Dunietz, B. D.; Beachy, M. D.; Cao, Y. X.; Whittington, D. A.; Lippard, S. J.; Friesner, R. A. J. Am. Chem. Soc. 2000, 122, 2828-2839.
63. Hay, P. J.; Wadt, W. R. J. Chem. Phys. 1985, 82, 270-283.
64. Wadt, W. R.; Hay, P. J. J. Chem. Phys. 1985, 82, 284-298.
65. Hay, P. J.; Wadt, W. R. J. Chem. Phys. 1985, 82, 299-310.
66. Dunning, T. H. J. Chem. Phys. 1989, 90, 1007-1023.
67. Noodleman, L. J. Chem. Phys. 1981, 74, 5737-5743.
68. Jaguar, version 4.1; Schrödinger, Inc.: Portland, OR, 2000.
69. Friesner, R. A.; Murphy, R. B.; Beachy, M. D.; Ringnalda, M. N.; Pollard, W. T.; Dunietz, B. D.; Cao, Y. X. J. Phys. Chem. A 1999, 103, 1913-1928.
70. 3 ligands were used to replace histidine residues. Before frequencies were computed, the positions of the capping hydrogen atoms from the glutamic acid residues and ammonia hydrogen atoms were optimized, while freezing the rest of the structure.
71. Use of a small model can lead to the introduction of artificial imaginary frequencies. Some small imaginary frequencies are due to bending and stretching modes of the capping or ammonia hydrogens. Other imaginary frequencies are merely numerical noise from the computation. Some imaginary frequencies are due to instabilities created in the small model upon removal from the protein environment. Given the inability at present to carry out frequency calculations within the QM/MM framework, this last problem is unavoidable when it surfaces. Careful examination of the vibrational modes allows these imaginary frequencies to be sifted through and structures to be identified as valid stationary points. The impact of the erroneous negative frequencies on the zero-point energy is minimal since low frequency vibrations contribute least to this quantity. Thermodynamic quantities are also little affected since excited vibrational modes are largely unpopulated at room temperature. Energetic errors thus caused are expected to be much smaller than those in the electronic energy from the DFT calculation.
72. Impact, version 1.7; Schrödinger, Inc.: Portland, OR, 2000.
73. Jorgensen, W. L.; Maxwell, D. S.; Tirado-Rives, J. J. Am. Chem. Soc. 1996, 118, 11225-11236.
74. Kaminski, G. A.; Friesner, R. A.; Tirado-Rives, J.; Jorgensen, W. L. J. Phys. Chem. B 2001, 105, 6474-6487.
75. Wirstam, M.; Gherman, B. F.; Guallar, V.; Murphy, R. B.; Friesner, R. A. Manuscript in preparation.
76. Friesner, R. A.; Baik, M.-H.; Guallar, V.; Gherman, B. F.; Wirstam, M.; Murphy, R. B.; Lippard, S. J. Coord. Chem. Rev. 2003, 238-239, 267-290.
77. Guallar, V.; Jacobson, M.; McDermott, A.; Friesner, R. A. J. Mol. Biol. 2004, 337, 227-239.
78. Gherman, B. F.; Goldberg, S. D.; Cornish, V. W.; Friesner, R. A. J. Am. Chem. Soc. 2004, 126, 7652-7664.
79. Cabani, S.; Gianni, P.; Mollica, V.; Lepori, L. J. Solution Chem. 1981, 10, 563-595.
80. Pye, C. C.; Ziegler, T. Theor. Chem. Acc. 1999, 101, 396-408.
81. Rosenzweig, A. C.; Brandstetter, H.; Whittington, D. A.; Nordlund, P.; Lippard, S. J.; Frederick, C. A. Proteins: Struct., Funct., Genet. 1997, 29, 141-152.
82. Elango, N.; Radhakrishnan, R.; Froland, W. A.; Wallar, B. J.; Earhart, C. A.; Lipscomb, J. D.; Ohlendorf, D. H. Protein Sci. 1997, 6, 556-568.
83. Liu, Y.; Nesheim, J. C.; Lee, S. K.; Lipscomb, J. D. J. Biol. Chem. 1995, 270, 24662-24665.
84. Skodje, R. T.; Truhlar, D. G. J. Phys. Chem. 1981, 85, 624-628.
85. Small changes to the endothermicity in the calculation of the transmission coefficient lead to trivial changes in the KIE for methane, making such an approximation very reasonable.
86. Lynch, B. J.; Fast, P. L.; Harris, M.; Truhlar, D. G. J. Phys. Chem. A 2000, 104, 4811-4815.
87. Guner, V.; Khuong, K. S.; Leach, A. G.; Lee, P. S.; Bartberger, M. D.; Houk, K. N. J. Phys. Chem. A 2003, 707, 11445-11459.
88. Warshel, A. Acc. Chem. Res. 2002, 35, 385-395.
89. Olsson, M. H. M.; Hong, G. Y.; Warshel, A. J. Am. Chem. Soc. 2003, 125, 5025-5039.
90. Theoretical free energies and rate constants are calculated at 25 °C rather than 20 °C, since the experimental values (see refs 79 and 80) for the free energies of solvation for the substrates were determined at 25 °C.