Molecular dynamics simulations of arachidonic acid-derived pentadienyl radical intermediate complexes with COX-1 and COX-2: Insights into oxygenation regio- and stereoselectivity

Biochemistry

Volumn 45, Issue 10, 2006, Pages 3206-3218

  Furse, Kristina E ^a,b   Pratt, Derek A ^a,c   Schneider, Claus ^a   Brash, Alan R ^a   Porter, Ned A ^a   Lybrand, Terry P ^a,b  

^a VANDERBILT UNIVERSITY   (United States)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c QUEEN S UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BIOSYNTHESIS; CELL CULTURE; DRUG THERAPY; ENZYME INHIBITION; ENZYMES; OXYGEN; STEREOCHEMISTRY; SUBSTRATES;

ASPIRIN; IBUPROFEN; OXYGEN CHANNELING; OXYGENATION; PENTADIENYL RADICAL INTERMEDIATE COMPLEXES; PROSTAGLANDIN; RADICAL TRAPPING; STEREOSELECTIVITY; STERIC SHIELDING; VIOXX;

MOLECULAR DYNAMICS;

ACETYLSALICYLIC ACID; ARACHIDONIC ACID; CELECOXIB; CYCLOOXYGENASE 1; CYCLOOXYGENASE 2; CYCLOOXYGENASE 2 INHIBITOR; IBUPROFEN; NONSTEROID ANTIINFLAMMATORY AGENT; RADICAL; ROFECOXIB; VALDECOXIB;

ARTICLE; COMPLEX FORMATION; CYCLIZATION; ENZYME ACTIVE SITE; ENZYME CONFORMATION; ENZYME MECHANISM; ENZYME SUBSTRATE COMPLEX; MOLECULAR DYNAMICS; OXYGEN TRANSPORT; OXYGENATION; PRIORITY JOURNAL; PROSTAGLANDIN SYNTHESIS; SIMULATION; SPIN TRAPPING; STEREOCHEMISTRY; THEORETICAL STUDY;

ARACHIDONIC ACID; BINDING SITES; COMPUTER SIMULATION; CYCLOOXYGENASE 1; CYCLOOXYGENASE 2; ENZYME STABILITY; MODELS, MOLECULAR; MOLECULAR CONFORMATION; OXYGEN; STEREOISOMERISM; SUBSTRATE SPECIFICITY;

EID: 33644868309     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi052338h     Document Type: Article

References (50)

1. Rouzer, C. A., and Marnett, L. J. (2003) Mechanism of free radical oxygenation of polyunsaturated fatty acids by cyclooxygenases, Chem. Rev. 103, 2239-2304.
2. Brash, A. R. (1999) Lipoxygenases: Occurrence, functions, catalysis, and acquisition of substrate, J. Biol. Chem. 274, 23679-23682.
3. Porter, N. A. (1986) Mechanisms for the autoxidation of polyunsaturated lipids, Acc. Chem. Res. 19, 262-268.
4. Funk, C. D. (2001) Prostaglandins and leukotrienes: Advances in eicosanoid biology, Science 294, 1871-1875.
5. Porter, N. A., Caldwell, S. E., and Mills, K. A. (1995) Mechanisms of free radical oxidation of unsaturated lipids, Lipids 30, 277-290.
6. Brash, A. (2000) Autoxidation of methyl linoleate: Identification of the bis-allylic 11-hydroperoxide, Lipids 35, 947-952.
7. Tallman, K. A., Pratt, D. A., and Porter, N. A. (2001) Kinetic products of linoleate peroxidation: rapid β-fragmentation of nonconjugated peroxyls, J. Am. Chem. Soc. 123, 11827-11828.
8. Bascetta, E., Gunstone, F. D., and Walton, J. C. (1983) An electron spin resonance study of fatty acids and esters. Part 1. Hydrogen abstraction from olefinine and acetylenic long-chain esters, J. Chem. Soc., Perkin Trans. 2, 603-613.
9. Porter, N. A., Weber, B. A., Weenen, H., and Khan, J. A. (1980) Autoxidation of polyunsaturated lipids. Factors controlling the stereochemistry of product hydroperoxides, J. Am. Chem. Soc. 102, 5597-5601.
10. Yin, H., Havrilla, C. M., Morrow, J. D., and Porter, N. A. (2002) Formation of isoprostane bicyclic endoperoxides from the autoxidation of cholesteryl arachidonate, J. Am. Chem. Soc. 124, 7745-7754.
11. +) ion spray-mass spectrometry of peroxidation products of cholesterol linoleate and cholesterol arachidonate: High-performance liquid chromatography-mass spectrometry analysis of peroxide products from polyunsaturated lipid autoxidation, J. Am. Chem. Soc. 122, 8042-8055.
12. Hecker, M., Ullrich, V., Fischer, C., and Meese, C. O. (1987) Identification of novel arachidonic acid metabolites formed by prostaglandin H synthase, Eur. J. Biochem. 169, 113-123.
13. Xiao, G., Tsai, A. L., Palmer, G., Boyar, W. C., Marshall, P. J., and Kulmacz, R. J. (1997) Analysis of hydroperoxide-induced tyrosyl radicals and lipoxygenase activity in aspirin-treated human prostaglandin H synthase-2, Biochemistry 36, 1836-1845.
14. van der Donk, W. A., Tsai, A. L., and Kulmacz, R. J. (2002) The cyclooxygenase reaction mechanism, Biochemistry 41, 15451-15458.
15. 1α, J. Biol. Chem. 242, 5336-5343.
16. Picot, D. (1998) The three-dimensional structure of cyclooxygenases, Lung Biol. Health Dis. 114 (Eicosanoids, Aspirin and Asthma), 161-186.
17. Malkowski, M. G., Ginell, S. L., Smith, W. L., and Garavito, R. M. (2000) The productive conformation of arachidonic acid bound to prostaglandin synthase, Science 289, 1933-1937.
18. Peng, S., Okeley, N. M., Tsai, A. L., Wu, G., Kulmacz, R. J., and van der Donk, W. A. (2001) Structural characterization of a pentadienyl radical intermediate formed during catalysis by prostaglandin H synthase-2, J. Am. Chem. Soc. 123, 3609-3610.
19. Peng, S., Okeley, N. M., Tsai, A. L., Wu, G., Kulmacz, R. J., and van der Donk, W. A. (2002) Synthesis of isotopically labeled arachidonic acids to probe reaction mechanism of prostaglandin H synthase, J. Am. Chem. Soc. 124, 10785-10796.
20. Kiefer, J. R., Pawlitz, J. L., Moreland, K. T., Stegeman, R. A., Hood, W. F., Gierse, J. K., Stevens, A. M., Goodwin, D. C., Rowlinson, S. W., Marnett, L. J., Stallings, W. C., and Kurumbail, R. G. (2000) Structural insights into the stereochemistry of the cyclooxygenase reaction, Nature 405, 97-101.
21. Wang, J., Cieplak, P., and Kollman, P. A. (2000) How well does a restrained electrostatic potential (RESP) model perform in calculating conformational energies of organic and biological molecules?, J. Comput. Chem. 21, 1049-1074.
22. Frisch, M. J., Trucks, G. W., Schlegel, H. B., Scuseria, G. E., Robb, M. A., Cheeseman, J. R., Zakrzewski, V. G., Montgomery, J. A., Jr., Stratmann, R. E., Burant, J. C., Dapprich, S., Millam, J. M., Daniels, A. D., Kudin, K. N., Strain, M. C., Farkas, O., Tomasi, J., Barone, V., Cossi, M., Cammi, R., Mennucci, B., Pomelli, C., Adamo, C., Clifford, S., Ochterski, J., Petersson, G. A., Ayala, P. Y., Cui, Q., Morokuma, K., Malic, D. K., Rabuck, A. D., Raghavachari, K., Foresman, J. B., Cioslowski, J., Ortiz, J. V., Baboul, A. G., Stefanov, B. B., Liu, G., Liashenko, A., Piskorz, P., Komaromi, I., Gomperts, R., Martin, R. L., Fox, D. J., Keith, T., Al-Laham, M. A., Peng, C. Y., Nanayakkara, A., Challacombe, M., Gill, P. M. W., Johnson, B., Chen, W., Wong, M. W., Andres, J. L., Gonzalez, C., Head-Gordon, M., Replogle, E. S., and Pople, J. A. (1998) Gaussian, Inc., Pittsburgh, PA.
23. Becke, A. D. (1993) Density-functional thermochemistry. III. The role of exact exchange, J. Chem. Phys. 98, 5648-5652.
24. Cornell, W. D., Cieplak, P., Bayly, C. I., Gould, I. R., Merz, K. M., Jr., Ferguson, D. M., Spellmeyer, D. C., Fox, T., Caldwell, J. W., and Kollman, P. A. (1995) A second generation force field for the simulation of proteins, nucleic acids, and organic molecules, J. Am. Chem. Soc. 117, 5179-5197.
25. Case, D. A., Pearlman, D. A., Caldwell, J. W., Cheatham, T. E., III, Wang, J., Ross, W. S., Simmerling, C. L., Darden, T. A., Merz, K. M., Stanton, R. V., Cheng, A. L., Vincent, J. J., Crowley, M., Tsui, V., Gohlke, H., Radmer, R. J., Duan, Y., Pitera, J., Massova, I., Seibel, G. L., Singh, U. C., Weiner, P. K., and Kollman, P. A. (2002) AMBER 7, University of California, San Francisco.
26. Berendsen, H. J. C., Grigera, J. R., and Straatsma, T. P. (1987) The missing term in effective pair potentials, J. Phys. Chem. 91, 6269-6271.
27. Ryckaert, J. P., Ciccotti, G., and Berendsen, H. J. C. (1977) Numerical-integration of Cartesian equations of motion of a system with constraints-molecular-dynamics of N-alkanes, J. Comput. Phys. 23, 327-341.
28. Berendsen, H. J. C., Postma, J. P. M., van Gunsteren, W. F., DiNola, A., and Haak, J. R. (1984) Molecular dynamics with coupling to an external bath, J. Chem. Phys. 81, 3684-3690.
29. Darden, T., York, D., and Pedersen, L. (1993) Patical mesh Ewald: An N-log(N) method for Ewald sums in large systems, J. Chem. Phys. 98, 10089-10092.
30. Callahan, T. J., Swanson, E., and Lybrand, T. P. (1996) MD display: An interactive graphics program for visualization of molecular dynamics trajectories, J. Mol. Graphics 14, 39-41.
31. Kumar, S., Rosenberg, J. M., Bouzida, D., Swendsen, R. H., and Kollman, P. A. (1995) Multidimensional free-energy calculations using the weighted histogram analysis method, J. Comput. Chem. 16, 1339-1350.
32. Grossfield, A. (2003) WHAM Version 1.2, Washington University, St. Louis, MO.
33. Sanner, M. F., Spehner, J.-C., and Olson, A. J. (1996) Reduced surface: An efficient way to compute molecular surfaces, Biopolymers 38, 305-320.
34. Philippsen, A. (2003) DINO: Visualizing Structural Biology (http://www.dino3d.org).
35. Pratt, D. A., Mills, J. H., and Porter, N. A. (2003) Theoretical calculations of carbon-oxygen bond dissociation enthalpies of peroxyl radicals formed in the autoxidation of lipids, J. Am. Chem. Soc. 125, 5801-5810.
36. Tsai, A., Palmer, G., Xiao, G., Swinney, D. C., and Kulmacz, R. J. (1998) Structural characterization of arachadonyl radicals formed by prostaglandin H synthase-2 and prostaglandin H synthase-1 reconstituted with mangano protoporphyrin IX, J. Biol. Chem. 273, 3888-3894.
37. Schneider, C., Boeglin, W. E., and Brash, A. R. (2004) Identification of two cyclooxygenase active site residues, leucine 384 and glycine 526, that control carbon ring cyclization in prostaglandin biosynthesis, J. Biol. Chem. 279, 4404-4414.
38. Thuresson, E. D., Lakkides, K. M., and Smith, W. L. (2000) Different catalytically competent arrangements of arachidonic acid within the cyclooxygenase active site of prostaglandin endoperoxide H synthase-1 lead to the formation of different oxygenated products, J. Biol. Chem. 275, 8501-8507.
39. Schreiner, K., and Berndt, A. (1974) EPR spectrum of a perpendicular benzyl radical, Angew. Chem., Int. Ed. 13, 144-145.
40. Regenstein, H., and Berndt, A. (1974) Homohyperconjugation in a perpendicular allyl radical, Angew. Chem., Int. Ed. 13, 145-146.
41. Tsai, A., Palmer, G., Wu, G., Peng, S., Okeley, N. M., van der Donk, W. A., and Kulmacz, R. J. (2002) Structural characterization of arachidonyl radicals formed by aspirin-treated prostaglandin H synthase-2, J. Biol. Chem. 277, 38311-38321.
42. Nelson, M. J., Cowling, R. A., and Seitz, S. P. (1994) Structual characterization of alkyl and peroxyl radicals in sollutions of purple lipoxygenase, Biochemistry 33, 4966-4973.
43. Minor, W., Steczko, J., Stec, B., Otwinowski, Z., Bolin, J. T., Walter, R., and Axelrod, B. (1996) Crystal structure of soybean lipoxygenase L-1 at 1.4 Å resolution, Biochemistsry 35, 10687-10701.
44. Knapp, M. J., Seebeck, F. P., and Klinman, J. P. (2001) Steric control of oxygenation regiochemistry in soybean lipoxygenase-1, J. Am. Chem. Soc. 123, 2931-2932.
45. Thuresson, E. D., Lakkides, K. M., Rieke, C. J., Sun, Y., Wingerd, B. A., Micielli, R., Mulichak, A. M., Malkowski, M. G., Garavito, R. M., and Smith, W. L. (2001) Prostaglandin endoperoxide H synthase-1: The functions of cyclooxygenase active site residues in the binding, positioning, and oxygenation of arachidonic acid, J. Biol. Chem. 276, 10347-10357.
46. Schneider, C., Boeglin, W. E., Prusakiewicz, J. J., Rowlinson, S. W., Marnett, L. J., Samel, N., and Brash, A. R. (2002) Control of prostaglandin stereochemistry at the 15-carbon by cyclooxygenases-1 and 2, J. Biol. Chem. 277, 478-485.
47. Porter, N. A., and Wujek, D. G. (1984) Autoxidation of polyunsaturated fatty acids, an expanded mechaistic study, J. Am. Chem. Soc. 106, 2626-2629.
48. Chenier, J. H. B., Furimsky, E., and Howard, J. A. (1974) Arrhenius parameters for reaction of the tert-butylperoxy and 2-ethyl-2-propylperoxy radicals with some nonhindered phenols, aromatic amines, and thiophenols, Can. J. Chem. 52, 3682-3688.
49. Burton, G. W., Doba, T., Gabe, E. J., Hughes, L., Lee, F. L., Prasad, L., and Ingold, K. U. (1985) Autoxidation of biological molecules. 4. Maximizing the antioxidant activity of phenols, J. Am. Chem. Soc. 107, 7053-7065.
50. Furse, K. E., Pratt, D. A., Porter, N. A., and Lybrand, T. P. (2006) Molecular dynamics simulations of arachidonic acid complexes with COX-1 and COX-2: Insights into equilibrium behavior, Biochemistry 45, 3189-3205.