Reaction pathway and free energy profiles for butyrylcholinesterase- catalyzed hydrolysis of acetylthiocholine

Biochemistry

Volumn 51, Issue 6, 2012, Pages 1297-1305

  Chen, Xi ^a,b   Fang, Lei ^b   Liu, Junjun ^a,b   Zhan, Chang Guo ^b  

^a CENTRAL CHINA NORMAL UNIVERSITY   (China)

^b University of Kentucky   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATION FREE ENERGY; BUTYRYLCHOLINESTERASE; CARBONYL CARBON; CATALYTIC MECHANISMS; COMPUTATIONAL PREDICTIONS; DEACYLATION; ENERGY PROFILE; EXPERIMENTAL KINETICS; FIRST-PRINCIPLES; MOLECULE BINDING; NUCLEOPHILIC ATTACK; PERIPHERAL ANIONIC SITE; PSEUDOBOND; QUANTUM MECHANICAL; RATE DETERMINING STEP; REACTION PATHWAYS; REACTION STEPS; SIDE-CHAINS; SUBSTRATE ACTIVATION; THIOCHOLINE; WATER MOLECULE;

ACYLATION; CALCULATIONS; CARBON; CATALYSIS; DISSOCIATION; ENERGY BARRIERS; ENZYMATIC HYDROLYSIS; FREE ENERGY; MOLECULAR MODELING; MOLECULES; QUANTUM THEORY;

SUBSTRATES;

ACETYLTHIOCHOLINE; CARBON; CARBONYL DERIVATIVE; CHOLINESTERASE; ESTER; NUCLEOPHILE; SERINE; WATER;

ACYLATION; ARTICLE; CATALYSIS; DEACYLATION; ENERGY; HYDROLYSIS; KINETICS; MOLECULAR MECHANICS; PRIORITY JOURNAL; QUANTUM MECHANICS;

ACETYLTHIOCHOLINE; ACYLATION; BUTYRYLCHOLINESTERASE; CATALYTIC DOMAIN; ENERGY METABOLISM; ENZYME ACTIVATION; HYDROGEN BONDING; HYDROLYSIS; QUANTUM THEORY; SUBSTRATE SPECIFICITY;

EID: 84863180859     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi201786s     Document Type: Article

References (63)

1. Fuxreiter, M. and Warshel, A. (1998) Origin of the catalytic power of acetylcholinesterase: Computer simulation studies J. Am. Chem. Soc. 120, 183-194 (Pubitemid 28046444)
2. Boeck, A. T., Schopfer, L. M., and Lockridge, O. (2002) DNA sequence of butyrylcholinesterase from the rat: expression of the protein and characterization of the properties of rat butyrylcholinesterase Biochem. Pharmacol. 63, 2101-2110 (Pubitemid 34756675)
3. Zhan, C. G. and Gao, D. Q. (2005) Catalytic mechanism and energy barriers for butyrylcholinesterase-catalyzed hydrolysis of cocaine Biophys. J. 89, 3863-3872
4. Masson, P., Froment, M. T., Gillon, E., Nachon, F., Lockridge, O., and Schopfer, L. M. (2008) Kinetic analysis of effector modulation of butyrylcholinesterase-catalysed hydrolysis of acetanilides and homologous esters FEBS J. 275, 2617-2631 (Pubitemid 351600100)
5. Mesulam, M. M., Guillozet, A., Shaw, P., Levey, A., Duysen, E. G., and Lockridge, O. (2002) Acetylcholinesterase knockouts establish central cholinergic pathways and can use butyrylcholinesterase to hydrolyze acetylcholine Neuroscience 110, 627-639 (Pubitemid 34270534)
6. Mesulam, M., Guillozet, A., Shaw, P., and Quinn, B. (2002) Widely spread butyrylcholinesterase can hydrolyze acetylcholine in the normal and Alzheimer brain Neurobiol. Dis. 9, 88-93 (Pubitemid 34174568)
7. Millard, C. B., Lockridge, O., and Broomfield, C. A. (1995) Design and expression of organophosphorus acid anhydride hydrolase activity in human butyrylcholinesterase Biochemistry 34, 15925-15933
8. Lockridge, O., Blong, R. M., Masson, P., Froment, M. T., Millard, C. B., and Broomfield, C. A. (1997) A single amino acid substitution, Gly117His, confers phosphotriesterase (organophosphorus acid anhydride hydrolase) activity on human butyrylcholinesterase Biochemistry 36, 786-795 (Pubitemid 27110958)
9. Pan, Y. M., Gao, D. Q., Yang, W. C., Cho, H., Yang, G. F., Tai, H. H., and Zhan, C. G. (2005) Computational redesign of human butyrylcholinesterase for anticocaine medication Proc. Natl. Acad. Sci. U. S. A. 102, 16656-16661 (Pubitemid 41688832)
10. Zhan, C. G., Zheng, F., and Landry, D. W. (2003) Fundamental reaction mechanism for cocaine hydrolysis in human butyrylcholinesterase J. Am. Chem. Soc. 125, 2462-2474 (Pubitemid 36512233)
11. Gao, D. Q., Cho, H., Yang, W. C., Pan, Y. M., Yang, G. F., Tai, H. H., and Zhan, C. G. (2006) Computational design of a human butyrylcholinesterase mutant for accelerating cocaine hydrolysis based on the transition-state simulation Angew. Chem., Int. Ed. 45, 653-657 (Pubitemid 43121468)
12. Zheng, F., Yang, W. C., Ko, M. C., Liu, J. J., Cho, H., Gao, D. Q., Tong, M., Tai, H. H., Woods, J. H., and Zhan, C. G. (2008) Most efficient cocaine hydrolase designed by virtual screening of transition states J. Am. Chem. Soc. 130, 12148-12155
13. Zheng, F. and Zhan, C.-G. (2008) Rational design of an enzyme mutant for anti-cocaine therapeutics J. Comput.-Aided Mol. Des. 22, 661-671
14. Zheng, F. and Zhan, C.-G. (2008) Structure-and-mechanism-based design and discovery of therapeutics for cocaine overdose and addiction Org. Biomol. Chem. 6, 836-843 (Pubitemid 351653352)
15. Gao, D. Q. and Zhan, C.-G. (2005) Modeling effects of oxyanion hole on the ester hydrolysis catalyzed by human cholinesterases J. Phys. Chem. B 109, 23070-23076 (Pubitemid 43010734)
16. Zhan, C.-G. (2009) Novel pharmacological approaches to treatment of drug overdose and addiction Expert Rev. Clin. Pharmacol. 2, 1-4
17. Yang, W., Pan, Y., Zheng, F., Cho, H., Tai, H.-H., and Zhan, C.-G. (2009) Free-Energy Perturbation Simulation on Transition States and Redesign of Butyrylcholinesterase Biophys. J. 96, 1931-1938
18. Pan, Y. M., Gao, D. Q., Yang, W. C., Cho, H., and Zhan, C.-G. (2007) Free energy perturbation (FEP) simulation on the transition states of cocaine hydrolysis catalyzed by human butyrylcholinesterase and its mutants J. Am. Chem. Soc. 129, 13537-13543 (Pubitemid 350071782)
19. Hamza, A., Cho, H., Tai, H.-H., and Zhan, C.-G. (2005) Molecular Dynamics Simulation of Cocaine Binding with Human Butyrylcholinesterase and Its Mutants J. Phys. Chem. B 109, 4776-4782 (Pubitemid 40429341)
20. Gao, D. Q. and Zhan, C.-G. (2006) Modeling evolution of hydrogen bonding and stabilization of transition states in the process of cocaine hydrolysis catalyzed by human butyrylcholinesterase Proteins 62, 99-110 (Pubitemid 43063008)
21. Yang, W., Xue, L., Fang, L., Chen, X., and Zhan, C.-G. (2010) Characterization of a high-activity mutant of human butyrylcholinesterase against (-)-cocaine Chem.-Biol. Interact. 187, 148-152
22. Yang, W., Pan, Y., Fang, L., Gao, D., Zheng, F., and Zhan, C.-G. (2010) Free Energy Perturbation Simulation on Transition States and High-Activity Mutants of Human Butyrylcholinesterase for (-)-Cocaine Hydrolysis J. Phys. Chem. B 114, 10889-10896
23. Brimijoin, S., Gao, Y., Anker, J. J., Gliddon, L. A., LaFleur, D., Shah, R., Zhao, Q. H., Singh, M., and Carroll, M. E. (2008) A cocaine hydrolase engineered from human butyrylcholinesterase selectively blocks cocaine toxicity and reinstatement of drug seeking in rats Neuropsychopharmacology 33, 2715-2725
24. Decker, M. (2005) Novel inhibitors of acetyl- and butyrylcholinesterase derived from the alkaloids dehydroevodiamine and rutaecarpine Eur. J. Med. Chem. 40, 305-313 (Pubitemid 40255773)
25. Sussman, J. L., Harel, M., Frolow, F., Oefner, C., Goldman, A., Toker, L., and Silman, I. (1991) Atomic-Structure of Acetylcholinesterase from Torpedo-Californica-a Prototypic Acetylcholine-Binding Protein Science 253, 872-879 (Pubitemid 21917225)
26. Saxena, A., Redman, A. M. G., Jiang, X. L., Lockridge, O., and Doctor, B. P. (1997) Differences in active site gorge dimensions of cholinesterases revealed by binding of inhibitors to human butyrylcholinesterase Biochemistry 36, 14642-14651 (Pubitemid 27524384)
27. Wlodek, S. T., Antosiewicz, J., and Briggs, J. M. (1997) On the mechanism of acetylcholinesterase action: The electrostatically induced acceleration of the catalytic acylation step J. Am. Chem. Soc. 119, 8159-8165 (Pubitemid 27390615)
28. Wang, Q. M., Jiang, H. L., Chen, J. Z., Chen, K. X., and Ji, R. Y. (1998) On the possible reaction pathway for the acylation of AChE-catalyzed hydrolysis of ACh: Semiempirical quantum chemical study Int. J. Quantum Chem. 70, 515-525
29. Vagedes, P., Rabenstein, B., Aqvist, J., Marelius, J., and Knapp, E. W. (2000) The deacylation step of acetylcholinesterase: Computer simulation studies J. Am. Chem. Soc. 122, 12254-12262 (Pubitemid 32062263)
30. Zhang, Y. K., Kua, J., and McCammon, J. A. (2002) Role of the catalytic triad and oxyanion hole in acetylcholinesterase catalysis: An ab initio QM/MM study J. Am. Chem. Soc. 124, 10572-10577 (Pubitemid 34977409)
31. Manojkumar, T. K., Cui, C. Z., and Kim, K. S. (2005) Theoretical insights into the mechanism of acetylcholinesterase-catalyzed acylation of acetylcholine J. Comput. Chem. 26, 606-611 (Pubitemid 40567106)
32. Suarez, D. and Field, M. J. (2005) Molecular dynamics simulations of human butyrylcholinesterase Proteins 59, 104-117 (Pubitemid 40316482)
33. Tachikawa, H., Igarashi, M., Nishihira, J., and Ishibashi, T. (2005) Ab initio model study on acetylcholinesterase catalysis: potential energy surfaces of the proton transfer reactions J. Photochem. Photobiol., B 79, 11-23 (Pubitemid 40425342)
34. Sant'Anna, C. M. R., Viana, A. D., and do Nascimento, N. M. (2006) A semiempirical study of acetylcholine hydrolysis catalyzed by Drosophila melanogaster acetylcholinesterase Bioorg. Chem. 34, 77-89
35. Suarez, D., Diaz, N., Fontecilla-Camps, J., and Field, M. J. (2006) A computational study of the deacylation mechanism of human butyrylcholinesterase Biochemistry 45, 7529-7543 (Pubitemid 43898663)
36. Zhou, Y., Wang, S., and Zhang, Y. (2010) Catalytic Reaction Mechanism of Acetylcholinesterase Determined by Born-Oppenheimer Ab Initio QM/MM Molecular Dynamics Simulations J. Phys. Chem. B 114, 8817-8825
37. Froede, H. C. and Wilson, I. B. (1984) Direct Determination of Acetyl-Enzyme Intermediate in the Acetylcholinesterase-Catalyzed Hydrolysis of Acetylcholine and Acetylthiocholine J. Biol. Chem. 259, 1010-1013
38. Nemukhin, A. V., Lushchekina, S. V., Bochenkova, A. V., Golubeva, A. A., and Varfolomeev, S. D. (2008) Characterization of a complete cycle of acetylcholinesterase catalysis by ab initio QM/MM modeling J. Mol. Model. 14, 409-416
39. Mesulam, M., Guillozet, A., Shaw, P., and Quinn, B. (2002) Widely spread butyrylcholinesterase can hydrolyze acetylcholine in the normal and Alzheimer brain Neurobiol. Dis. 9, 88-93 (Pubitemid 34174568)
40. Eriksson, H. and Augustinsson, K. B. (1979) Mechanisitic model for butyrylcholinesterase Biochim. Biophys. Acta 567, 161-173
41. Komers, K., Cegan, A., and Link, M. (2002) Kinetics and mechanism of hydrolysis of acetylthiocholine by butyrylcholine esterase Z. Naturforsch., C: J. Biosci. 57, 1072-1077 (Pubitemid 36137354)
42. Masson, P., Froment, M. T., Bartels, C. F., and Lockridge, O. (1996) Asp70 in the peripheral anionic site of human butyrylcholinesterase Eur. J. Biochem. 235, 36-48 (Pubitemid 26045418)
43. Tormos, J. R., Wiley, K. L., Seravalli, J., Nachon, F., Masson, P., Nicolet, Y., and Quinn, D. M. (2005) The reactant state for substrate-activated turnover of acetylthiocholine by butyrylcholinesterase is a tetrahedral intermediate J. Am. Chem. Soc. 127, 14538-14539 (Pubitemid 41510971)
44. Wiley, K. L., Tormos, J. R., and Quinn, D. M. (2010) A secondary isotope effect study of equine serum butyrylcholinesterase-catalyzed hydrolysis of acetylthiocholine Chem.-Biol. Interact. 187, 124-127
45. Shafferman, A., Velan, B., Ordentlich, A., Kronman, C., Grosfeld, H., Leitner, M., Flashner, Y., Cohen, S., Barak, D., and Ariel, N. (1992) Substrate-Inhibition of Acetylcholinesterase-Residues Affecting Signal Transduction from the Surface to the Catalytic Center EMBO J. 11, 3561-3568
46. Gao, Y., LaFleur, D., Shah, R., Zhao, Q. H., Singh, M., and Brimijoin, S. (2008) An albumin-butyrylcholinesterase for cocaine toxicity and addiction: Catalytic and pharmacokinetic properties Chem.-Biol. Interact. 175, 83-87
47. Chen, X., Fang, L., Liu, J. J., and Zhan, C. G. (2011) Reaction Pathway and Free Energy Profile for Butyrylcholinesterase-Catalyzed Hydrolysis of Acetylcholine J. Phys. Chem. B 115, 1315-1322
48. Eriksson, H. and Augustinsson, K. B. (1979) Mechanistic Model for Butyrylcholinesterase Biochim. Biophys. Acta 567, 161-173
49. Komers, K., Cegan, A., and Link, M. (2002) Kinetics and mechanism of hydrolysis of acetylthiocholine by butyrylcholine esterase Z. Naturforsch., C: J. Biosci. 57, 1072-1077 (Pubitemid 36137354)
50. Gao, Y., LaFleur, D., Shah, R., Zhao, Q. H., Singh, M., and Brimijoin, S. (2008) An albumin-butyrylcholinesterase for cocaine toxicity and addiction: Catalytic and pharmacokinetic properties Chem.-Biol. Interact. 175, 83-87
51. Zhang, Y. K. (2005) Improved pseudobonds for combined ab initio quantum mechanical/molecular mechanical methods J. Chem. Phys. 122, 024114
52. Zhang, Y. K., Lee, T. S., and Yang, W. T. (1999) A pseudobond approach to combining quantum mechanical and molecular mechanical methods J. Chem. Phys. 110, 46-54
53. Hu, P. and Zhang, Y. K. (2006) Catalytic mechanism and product specificity of the histone lysine methyltransferase SET7/9: An ab initio QM/MM-FE study with multiple initial structures J. Am. Chem. Soc. 128, 1272-1278 (Pubitemid 43190640)
54. Zhang, Y. K., Liu, H. Y., and Yang, W. T. (2000) Free energy calculation on enzyme reactions with an efficient iterative procedure to determine minimum energy paths on a combined ab initio QM/MM potential energy surface J. Chem. Phys. 112, 3483-3492
55. Zhang, Y. K. (2006) Pseudobond ab initio QM/MM approach and its applications to enzyme reactions Theor. Chem. Acc. 116, 43-50
56. Liu, J. J., Hamza, A., and Zhan, C. G. (2009) Fundamental Reaction Mechanism and Free Energy Profile for (-)-Cocaine Hydrolysis Catalyzed by Cocaine Esterase J. Am. Chem. Soc. 131, 11964-11975
57. Liu, J. J., Zhang, Y. K., and Zhan, C. G. (2009) Reaction Pathway and Free-Energy Barrier for Reactivation of Dimethylphosphoryl-Inhibited Human Acetylcholinesterase J. Phys. Chem. B 113, 16226-16236
58. Poyner, R. R., Larsen, T. M., Wong, S. W., and Reed, G. H. (2002) Functional and structural changes due to a serine to alanine mutation in the active-site flap of enolase Arch. Biochem. Biophys. 401, 155-163 (Pubitemid 34848617)
59. Cisneros, G. A., Wang, M., Silinski, P., Fitzgerald, M. C., and Yang, W. T. (2004) The protein backbone makes important contributions to 4-oxalocrotonate tautomerase enzyme catalysis: Understanding from theory and experiment Biochemistry 43, 6885-6892 (Pubitemid 38720506)
60. Metanis, N., Brik, A., Dawson, P. E., and Keinan, E. (2004) Electrostatic interactions dominate the catalytic contribution of Arg39 in 4-oxalocrotonate tautomerase J. Am. Chem. Soc. 126, 12726-12727 (Pubitemid 39372273)
61. Frisch, M. J., Trucks, G. W., Schlegel, H. B., Scuseria, G. E., Robb, M. A., Cheeseman, J. R., Montgomery, J., J., A., Vreven, T., Kudin, K. N., Burant, J. C., Millam, J. M., Iyengar, S. S., Tomasi, J., Barone, V., Mennucci, B., Cossi, M., Scalmani, G., Rega, N., Petersson, G. A., Nakatsuji, H., Hada, M., Ehara, M., Toyota, K., Fukuda, R., Hasegawa, J., Ishida, M., Nakajima, T., Honda, Y., Kitao, O., Nakai, H., Klene, M., Li, X., Knox, J. E., Hratchian, H. P., Cross, J. B., Bakken, V., Adamo, C., Jaramillo, J., Gomperts, R., Stratmann, R. E., Yazyev, O., Austin, A. J., Cammi, R., Pomelli, C., Ochterski, J. W., Ayala, P. Y., Morokuma, K., Voth, G. A., Salvador, P., Dannenberg, J. J., Zakrzewski, V. G., Dapprich, S., Daniels, A. D., Strain, M. C., Farkas, O., Malick, D. K., Rabuck, A. D., Raghavachari, K., Foresman, J. B., Ortiz, J. V., Cui, Q., Baboul, A. G., Clifford, S., Cioslowski, J., Stefanov, B. B., Liu, G., Liashenko, A., Piskorz, P., Komaromi, I., 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., Gonzalez, C., and and Pople, J. A. (2004) Gaussian 03, Revision C.02, Gaussian, Inc., Wallingford, CT.
62. Case, D. A., Darden, T. A., T.E. Cheatham, I., Simmerling, C. L., Wang, J., Duke, R. E., Luo, R., Merz, K. M., Wang, B., Pearlman, D. A., Crowley, M., Brozell, S., Tsui, V., Gohlke, H., Mongan, J., Hornak, V., Cui, G., Beroza, P., Schafmeister, C., Caldwell, J. W., Ross, W. S., and Kollman, P. A. (2004) AMBER8, University of California, San Francisco.
63. Alvarez-Idaboy, J. R., Galano, A., Bravo-Perez, G., and Ruiz, M. E. (2001) Rate constant dependence on the size of aldehydes in the NO3+ aldehydes reaction. An explanation via quantum chemical calculations and CTST J. Am. Chem. Soc. 123, 8387-8395 (Pubitemid 32916413)