Direct correlation between molecular dynamics and enzymatic stability: A comparative neutron scattering study of native human butyrylcholinesterase and its "aged" soman conjugate

Biophysical Journal

Volumn 96, Issue 4, 2009, Pages 1489-1494

  Gabel, F ^a   Masson, P ^a   Froment, M T ^b   Doctor, B P ^c   Saxena, A ^c   Silman, I ^d   Zaccai, G ^a,e   Weik, M ^a  

^a INSTITUT DE BIOLOGIE STRUCTURALE   (France)

^b CENTRE DE RECHERCHES   (France)

^c WALTER REED ARMY INSTITUTE OF RESEARCH   (United States)

^d WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^e INSTITUT LAUE LANGEVIN   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLINESTERASE; SOMAN;

ARTICLE; CALORIMETRY; DENATURATION; DIAGNOSTIC ACCURACY; DIFFERENTIAL SCANNING CALORIMETRY; ENTHALPY; ENTROPY; ENZYME INHIBITION; ENZYME PURIFICATION; ENZYME STABILITY; FREEZE DRYING; HUMAN; INTERMETHOD COMPARISON; MACROMOLECULE; MATHEMATICAL ANALYSIS; MEAN SQUARE DISPLACEMENT; MOLECULAR DYNAMICS; MOLECULAR STABILITY; NEUTRON SCATTERING; PROTEIN DENATURATION; QUANTITATIVE ANALYSIS; SIGNAL NOISE RATIO; TEMPERATURE MEASUREMENT; THERMODYNAMICS; ALGORITHM; CHEMICAL MODEL; CHEMISTRY; COMPARATIVE STUDY; NEUTRON DIFFRACTION; PROTEIN CONFORMATION; SPECTROSCOPY; TEMPERATURE;

ALGORITHMS; BUTYRYLCHOLINESTERASE; CALORIMETRY, DIFFERENTIAL SCANNING; ENTROPY; ENZYME STABILITY; HUMANS; MODELS, CHEMICAL; NEUTRON DIFFRACTION; PROTEIN CONFORMATION; PROTEIN DENATURATION; SOMAN; SPECTRUM ANALYSIS; TEMPERATURE; THERMODYNAMICS;

EID: 62649108471     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2008.10.029     Document Type: Article

References (32)

1. Payne, C. S., M. Saeed, and A. D. Wolfe. 1989. Ligand stabilization of cholinesterases. Biochim. Biophys. Acta. 999:46-51. (Pubitemid 19264347)
2. Gabel, F., M. Weik, P. Masson, F. Renault, D. Fournier, et al. 2005. Effects of soman inhibition and of structural differences on cholinesterase molecular dynamics: a neutron scattering study. Biophys. J. 89:3303-3311.
3. Rochu, D., C. Clery-Barraud, F. Renault, A. Chevalier, C. Bon, et al. 2006. Capillary electrophoresis versus differential scanning calorimetry for the analysis of free enzyme versus enzyme-ligand complexes: in the search of the ligand-free status of cholinesterases. Electrophoresis. 2:442-451.
4. Ollis, D. L., E. Cheah, M. Cygler, B. Dijkstra, F. Frolow, et al. 1992. The α/β-hydrolase fold. Protein Eng. 5:197-211.
5. Nicolet, Y., O. Lockridge, P. Masson, J. C. Fontecilla-Camps, and F. Nachon. 2003. Crystal structure of human butyryl cholinesterase and of its complexes with substrate and products. J. Biol. Chem. 278:41141-41147. (Pubitemid 37280939)
6. Silman, I., and J. L. Sussmann. 2005. Acetylcholinesterase: 'classical' and 'non-classical' functions and pharmacology. Curr. Opin. Pharmacol. 5:293-302.
7. Quinn, D. M. 1987. Acetylcholinesterase: enzyme structure, reaction dynamics, and virtual transition states. Chem. Rev. 87:955-979.
8. Darvesh, S., D. A. Hopkins, and C. Geula. 2003. Neurobiology of butyrylcholinesterase. Nat. Rev. Neurosci. 4:131-138. (Pubitemid 37271383)
9. Duysen, E. G., B. Li, S. Darvesh, and O. Lockridge. 2007. Sensitivity of butyrylcholinesterase knockout mice to (-)-huperzine A and donepezil suggests humans with butyrylcholinesterase deficiency may not tolerate these Alzheimer's disease drugs and indicates butyrylcholinesterase function in neurotransmission. Toxicology. 233:60-69. (Pubitemid 46509686)
10. Li, B., M. Sedlacek, I. Manoharam, R. Boopathy, E. G. Duysen, et al. 2005. Butyrylcholinesterase, paraoxonase, and albumin esterase but not carboxylesterase, are present in human plasma. Biochem. Pharmacol. 70:1673-1684.
11. Doctor, B. P., and A. Saxena. 2005. Bioscavengers for the protection of humans against organophosphate toxicity. Chem. Biol. Interact. 157-158:167-171. (Pubitemid 41757647)
12. Huang, Y. -J., Y. Huang, H. Baldassarre, B. Wang, A. Lazaris, et al. 2007. Recombinant human butyrylcholinesterase from milk of transgenic animals to protect against organophosphate poisoning. Proc. Natl. Acad. Sci. USA. 104:13603-13608.
13. Ashani, Y., and S. Pistinner. 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.
14. Tara, S., T. P. Straatsma, and J. A. McCammon. 1999. Mouse acetylcholinesterase unliganded and in complex with huperzine A: a comparison of molecular dynamics simulations. Biopolymers. 50:35-43.
15. Millard, C. B., G. Kryger, A. Ordentlich, H. M. Greenblatt, M. Harel, et al. 1999. Crystal structures of aged phosphorylated acetylcholinesterase: nerve agent reaction products at the atomic level. Biochemistry. 38:7032-7039.
16. Masson, P., and J. Goasdoue. 1986. Evidence that the conformational stability of "aged" organophosphate-inhibited cholinesterase is altered. Biochim. Biophys. Acta. 14:304-313.
17. Masson, P., C. Cléry, P. Guerra, A. Redslob, C. Albaret, et al. 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.
18. Grunwald, J., D. Marcus, Y. Papier, L. Raveh, Z. Pittel, et al. 1997. Large-scale purification and long-term stability of human butyrylcholinesterase: a potential bioscavenger drug. J. Biochem. Biophys. Methods. 34:123-135.
19. Gabel, F., M. Weik, B. P. Doctor, A. Saxena, D. Fournier, et al. 2004. The influence of solvent composition on global dynamics of human butyrylcholinesterase powders: a neutron scattering study. Biophys. J. 86:3152-3165.
20. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 227:680-685.
21. Millard, C. B., and C. A. Broomfield. 1995. Anticholinesterases: medical applications of neurochemical principles. J. Neurochem. 64:1909-1918.
22. Anderson, I. S., and R. Nelson. 1985. User's Guide for Program 'SQW'. Institut Laue-Langevin Internal Report No. ILL85AN8T, Grenoble, France.
23. Bée, M. 1988. Quasielastic Neutron Scattering. Adam Hilger, Bristol, UK.
24. Combet, J., B. Frick, O. Losserand, M. Gamon, and B. Guerard. 2000. Simultaneous diffraction and inelastic scattering on the backscattering instrument IN16. Phys. B Cond. Matt. 283:380-385.
25. Smith, J. C. 1991. Protein dynamics: comparison of simulations with inelastic neutron scattering experiments. Q. Rev. Biophys. 24:227-291.
26. Guinier, A., and G. Fournet. 1955. Small Angle Scattering of X-Rays. John Wiley & Sons, New York, London.
27. Zaccai, G. 2000. How soft is a protein? A protein dynamics force constant measured by neutron scattering. Science. 288:1604-1607. (Pubitemid 30387420)
28. Bicout, D. J., and G. Zaccai. 2001. Protein flexibility from the dynamical transition: a force constant analysis. Biophys. J. 80:1115-1123.
29. Frauenfelder, H., F. Parak, and R. D. Young. 1988. Conformational substrates in proteins. Annu. Rev. Biophys. Biophys. Chem. 17:451-479.
30. Perez, J., J. -M. Zanotti, and D. Durand. 1999. Evolution of the internal dynamics of two globular proteins from dry powder to solution. Biophys. J. 77:454-469. (Pubitemid 29305242)
31. Gabel, F. 2005. Protein dynamics in solution and powder measured by incoherent elastic neutron scattering: the influence of Q-range and energy resolution. Eur. Biophys. J. 34:1-12.
32. Zaks, A., and A. M. Klibanov. 1985. Enzyme-catalyzed processes in organic solvents. Proc. Natl. Acad. Sci. USA. 82:3192-3196. (Pubitemid 15029572)