Rate-determining step of butyrylcholinesterase-catalyzed hydrolysis of benzoylcholine-and benzoylthiocholine: Volumetric study of wild-type and D70G mutant behaviour

European Journal of Biochemistry

Volumn 271, Issue 10, 2004, Pages 1980-1990

  Masson, Patrick ^a   Bec, Nicole ^b   Froment, Marie Thérèse ^a   Nachon, Florian ^a,c   Balny, Claude ^b   Lockridge, Oksana ^c   Schopfer, Lawrence M ^c  

^a CENTRE DE RECHERCHES   (France)

^b INSERM   (France)

^c UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

Benzoylcholine; Benzoylthiocholine; Butyrylcholinesterase; Pressure; Volume change

Indexed keywords

ANION; BENZOYLCHOLINE; BENZOYLTHIOCHOLINE; CHOLINE DERIVATIVE; CHOLINESTERASE; DYFLOS; MUTANT PROTEIN; UNCLASSIFIED DRUG; WATER;

ACYLATION; ARTICLE; ATMOSPHERIC PRESSURE; CATALYSIS; DEACYLATION; ENZYME BINDING; ENZYME PHOSPHORYLATION; ENZYME SUBSTRATE; HYDROLYSIS; HYDROSTATIC PRESSURE; HYPERBARISM; MOLECULE; MUTANT; NONLINEAR SYSTEM; PRIORITY JOURNAL; STEADY STATE; VOLUMETRY; WILD TYPE;

AMINO ACID SUBSTITUTION; ATMOSPHERIC PRESSURE; BENZOYLCHOLINE; BINDING SITES; BUTYRYLCHOLINESTERASE; CATALYSIS; ENZYME ACTIVATION; HUMANS; HYDROLYSIS; ISOFLUROPHATE; KINETICS; MODELS, MOLECULAR; PHOSPHORYLATION; PROTEIN BINDING; RECOMBINANT PROTEINS;

EID: 2442713750     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1432-1033.2004.04110.x     Document Type: Article

References (47)

1. Massoulié, J., Pezzementi, L., Bon, S., Krejci, E. & Vallette, F.-M. (1993) Molecular and cellular biology of cholinesterases. Prog. Neurobiol. 41, 31-91.
2. Li, B., Stribley, J.A., Ticu, A., Xie, W., Schopfer, L.M., Hammond, P., Brimijoin, S., Hinrichs, S.H. & Lockridge, O. (2000) Abundant tissue butyrylcholinesterase and its possible function in the acetylcholinesterase knockout mouse. J. Neurochem. 75, 1320-1331.
3. Mesulam, M.M., Guillozet, A., Shaw, P., Levey, A., Duysen, E.G. & Lockridge, O. (2002) Acetylcholinesterase knockouts establish central cholinergic pathways and can use butyrylcholinesterase to hydrolyze acetylcholine. Neuroscience 110, 627-639.
4. Darvesh, S., Hopkins, D.A. & Geula, C. (2003) Neurobiology of butyrylcholinesterase. Nature Rev. Neurosci. 4, 131-138.
5. 3H-bambuterol, a carbamate prodrug of terbutaline, in blood from humans and laboratory animals in vitro. Biochem. Pharmacol. 37, 3867-3876.
6. Gilmer, G.F., Moriarty, L.M., Lally, M.N. & Clancy, J.M. (2002) Isosorbide-based aspirin prodrugs. II. Hydrolysis kinetics of isosorbide diaspirinate. Eur. J. Pharm. Sci. 16, 297-304.
7. Sun, H., Yazals, J.M., Lockridge, O., Schopfer, L.M., Brimijoin, S. & Pang, Y.-P. (2001) Predicted Michaelis-Menten complexes of cocaine- butyrylcholinesterase. J. Biol. Chem. 276, 9330-9336.
8. Cerasoli, D.M. & Lenz, D.L. (2002) Nerve agents bioscavengers: protection with reduced behavioral effects. Milit. Psychol. 14, 121-143.
9. Doctor, B.P. (2003) Butyrylcholinesterase: its use for prophylaxis of organophosphate exposure. In Butyrylcholinesterase, its Function and Inhibitors (Giacobini, E., ed.), pp. 163-177. Martin Dunitz, London.
10. Ashani, Y. & Pistinner, S. (2004) Estimation of the upper limit of human butyrylcholinesterase dose required for protection against organophosphates toxicity: a mathematically based toxicokinetic model. Toxicol. Sci. 77, 358-367.
11. Sussman, J.L., Harel, M., Frolow, F., Oefner, C., Goldman, A., Toker, L. & Silman, I. (1991) Atomic structure of acetylcholinesterase from Torpedo californica: a prototypic acetylcholine-binding protein. Science 253, 872-879.
12. Nicolet, Y., Lockridge, O., Masson, P., Fontecilla-Camp, J.-C. & Nachon, F. (2003) Crystal structure of human butyrylcholinesterase and of its complexes with substrate and products. J. Biol. Chem. 278, 41141-41147.
13. Masson, P., Legrand, P., Bartels, C.F., Froment, M.-T., Schopfer, L.M. & Lockridge, L. (1997) Role of aspartate 70 and tryptophan 82 in binding of succinyldithiocholine to human butyrylcholinesterase. Biochemistry 36, 2266-2277.
14. Masson, P., Schopfer, L.M., Bartels, C.F., Froment, M.-T., Ribes, F., Nachon, F. & Lockridge, O. (2002) Substrate activation in acetylcholinesterase induced by low pH or mutation in the π-cation subsite. Biochim. Biophys. Acta 1594, 313-324.
15. Masson, P., Nachon, F., Bartels, C.F., Froment, M.-T., Ribes, F., Matthews, C. & Lockridge, O. (2003) High activity of human butyrylcholinesterase at low pH in the presence of excess butyrylthiocholine. Eur J. Biochem. 270, 315-324.
16. Johnson, J.L., Cusack, B., Davies, M.P., Fauq, A. & Rosenberry, T.L. (2003) Unmasking tandem site interaction in human acetylcholinesterase. Substrate activation with a cationic acetanilide substrate. Biochemistry 42, 5438-5452.
17. Masson, P., Froment, M.T., Fort, S., Ribes, F., Bec, N., Balny, C. & Schopfer, L.M. (2002) Butyrylcholinesterase-catalyzed hydrolysis of N-methylindoxyl acetate: analysis of volume changes upon reaction and hysteretic behavior. Biochim. Biophys. Acta 1597, 229-243.
18. Masson, P., Goldstein, B.N., Debouzy, J.-C, Froment, M.-Th, Lockridge, O. & Schopfer, L.M. (2004) Damped oscillatory hysteretic behaviour of butyrylcholinesterase with benzoylcholine as substrate. Eur. J. Biochem. 271, 220-234.
19. Morild, E. (1981) The theory of pressure effects on enzymes. Adv. Prot. Chem. 34, 93-163.
20. Balny, C., Masson, P. & Heremans, K. (2002) Frontiers in high pressure biophysics and biochemistry. Biochim. Biophys. Acta 1595, 1-403.
21. Lockridge, O., Blong, R.M., Masson, P., Froment, M.-T., Millard, C.B. & Broomfield, C.A. (1997) A single amino acid substitution, Gly117His, confers phosphotriesterase (organophosphorus acid anhydride hydrolase) activity on human butyrylcholinesterase. Biochemistry 36, 786-795.
22. Amitai, G., Moorad, D., Adani, R. & Doctor, B.P. (1998) Inhibition of acetylcholinesterase and butyrylcholinesterase by chlorpyrifos-oxon. Biochem. Pharmacol. 56, 293-299.
23. Kitamura, Y. & Itoh, T. (1987) Reaction volume of protonic ionization for buffering agent. Prediction of pressure dependence of pH and pOH. J. Soln. Chem. 16, 715-725.
24. Ellman, G.L., Courtney, K.D., Andres, V. & Featherstone, R.M. (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem. Pharmacol. 7, 88-95.
25. Stojan, J. & Pavlic, M.R. (1992) Velocity of Ellman's reaction and its implication for kinetic studies in the millisecond time range. Neurochem. Res. 17, 1207-1210.
26. Stojan, J. (2001) Slow detection reaction can mimic initial inhibition of an enzymic reaction. J. Enz. Inhib. 16, 89-94.
27. Balny, C., Saldana, J.-L. & Dahan, N. (1984) High-pressure stopped-flow spectrophotometry at low temperatures. Anal. Biochem. 139, 178-189.
28. Hart, G.F. & O'Brien, R.D. (1974) Stopped-flow studies of the inhibition of acetylcholinesterase by organophosphates in the presence of substrate. Pestic. Biochem. Physiol. 4, 239-244.
29. Morris, G.M., Goodsell, D.S., Halliday, R.S., Huey, R., Hart, W.E., Belew, R.K. & Olson, A.J. (1998) Automated docking using a Lamarckian genetic algorithm and an empirical binding free energy function. J. Comput. Chem. 19, 1639-1662.
30. Van Eldik, R., Asana, T. & Le Noble, W.J. (1989) Activation volumes in solution. Chem. Rev. 89, 549-688.
31. Masson, P. & Balny, C. (1990) Conformational plasticity of butyrylcholinesterase as revealed by high pressure experiments. Biochim. Biophys. Acta 1041, 223-231.
32. Kauzmann, W. (1959) Some factors in the interpretation of protein denaturation. Adv. Prot. Chem. 14, 1-63.
33. Cooper, A. (1976) Thermodynamic fluctuations in protein molecules. Proc. Natl Acad. Sci. USA 73, 2740-2741.
34. Kharakoz, D.P. (2000) Protein compressibility, dynamics and pressure. Biophys. J. 79, 511-525.
35. Taulier, N. & Chalikian, T.V. (2002) Compressibility of protein transitions. Biochim. Biophys. Acta 1595, 48-70.
36. Chalikian, T.V. (2003) Volume tric properties of proteins. Annu. Rev. Biomol. Struct. 32, 207-235.
37. Masson, P., Clery, C., Guerra, P., Redslob, A., Albaret, C. & Fortier, P.-L. (1999) Hydration change during the aging of phosphorylated human butyrylcholinesterase: importance of residues aspartate-70 and glutamate-197 in the water network as probed by hydrostatic and osmotic pressures. Biochem. J. 343, 361-369.
38. Millard, C.B., Kryger, G., Ordentlich, A., Greenblatt, H.M., Harel, M., Raves, M.L., Segall, Y., Barak, D., Shafferman, A., Silman, I. & Sussman, J.L. (1999) Crystal structures of aged phosphonylated acetylcholinesterase: nerve agent reaction produes at the atomic level. Biochemistry 38, 7032-7039.
39. Ordentlich, A., Barak, D., Kronman, C., Ariel, N., Segall, Y., Velan, B. & Shafferman, A. (1998) Functional characteristics of the oxyanion hole in human acetylcholinesterase. J. Biol. Chem. 273, 19509-19517.
40. Zhang, Y., Kua, J. & 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.
41. Tanigushi, Y. & Makimoto, S. (1988) High pressure studies of enzyme catalysis. J. Mol. Catal. 47, 323-324.
42. Butz, P., Greulich, K.O. & Ludwig, H. (1988) Volume changes during enzyme reactions: indications of enzyme pulsation during fumarase catalysis. Biochemistry 27, 1556-1563.
43. Gekko, K. (2002) Compressibility gives new insight into protein dynamics and enzyme function. Biochim. Biophys. Acta 1595, 382-386.
44. Malany, S., Sawai, M., Sikorski, R.S., Seravalli, J., Quinn, D.M., Radic, Z., Taylor, P., Chronman, C., Velan, B. & Shafferman, A. (2000) Transition state structure and rate determination foor the acylation stage of acetylcholinesterase catalyzed hydrolysis of (acetylthio) choline. J. Am. Chem. Soc. 122, 2981-2987.
45. Fuxeiter, M. & Warshel, A. (1998) Origin of the catalytic power of acetylcholinesterase: computer simulation studies. J. Am. Chem. Soc. 120, 183-194.
46. Harel, M., Quinn, D.M., Nair, H.K., Silman, I. & Sussman, J.L. (1996) The X-ray structure of a transition state analog complex reveals the molecular origins of the catalytic power and stubstrate specificity of acetylcholinesterase. J. Am. Chem. Soc. 118, 2340-2346.
47. Shefter, E. & Mautner, H.G. (1969) Acetylcholine and its thiolester and selenoester analogs: conformation, electron distribution, and biological activity. Proc. Natl Acad. Sci. USA 63, 1253-1260.