Structure, activities and biomedical applications of human butyrylcholinesterase

Protein and Peptide Letters

Volumn 16, Issue 10, 2009, Pages 1215-1224

  Masson, Patrick ^a   Carletti, Eugénie ^a   Nachon, Florian ^a  

^a CENTRE DE RECHERCHES   (France)

Author keywords

Acetylcholinesterase; Bioscavenger; Biosensor; Butyrylcholinesterase; Cocaine; Organophosphate; Protein engineering

Indexed keywords

CHOLINESTERASE; CHOLINESTERASE INHIBITOR;

APNEA; ARTICLE; CHEMISTRY; ENZYME ACTIVE SITE; ENZYME SPECIFICITY; ENZYMOLOGY; GENETIC PROCEDURES; HUMAN; INSTRUMENTATION; KINETICS; METABOLISM; METHODOLOGY; PROTEIN TERTIARY STRUCTURE; STRUCTURE ACTIVITY RELATION;

APNEA; BIOSENSING TECHNIQUES; BUTYRYLCHOLINESTERASE; CATALYTIC DOMAIN; CHOLINESTERASE INHIBITORS; HUMANS; KINETICS; PROTEIN STRUCTURE, TERTIARY; STRUCTURE-ACTIVITY RELATIONSHIP; SUBSTRATE SPECIFICITY;

EID: 67650537353     PISSN: 09298665     EISSN: None     Source Type: Journal    
DOI: 10.2174/092986609789071207     Document Type: Article

References (102)

1. Mesulam, MM.; Guillozet, A.; Shaw, P.; Levey, A.; Duysen, EG.; Lockridge, O. Acetylcholinesterase knockouts establish central cholinergic pathways and can use butyrylcholinesterase to hydrolyze acetylcholine. Neuroscience, 2002, 110, 627-639.
2. Massoulié, J.; Perrier, N.; Noureddine, H.; Liang, D.; Bon, S. Old and new questions about cholinesterases. Chem. Biol. Interact., 2008, 175, 30-44.
3. Chatonnet, A.; Lockridge, O. Comparison of butyrylcholinesterase and acetylcholinesterase. Biochem. J., 1989, 260, 625-34.
4. Mack, A.; Robitzki, A. The key role of butyrylcholinesterase during neurogenesis and neural disorders: an antisense-5'butyrylcholinesterase-DNA study. Progr. Neurobiol., 2000, 60, 607-28.
5. Lockridge, O. Genetic variants of human serum cholinesterase influence metabolism of the muscle relaxant succinylcholine. Pharmac. Ther., 1990, 47, 35-60.
6. Lockridge, O.; Masson, P. Pesticides and susceptible populations: people with butyrylcholinesterase genetic variants may be at risk. NeuroToxicol., 2000, 21, 113-26.
7. Allderdice, P.W.; Gardner, H.A.R.; Galutira, D.; Lockridge, O.; LaDu, B.N.; McAlpine, P.J. The cloned butyrylcholinesterase (BCHE) gene maps to a single chromosome site, 3q26. Genomics, 1991, 11, 452-4.
8. Masson, P.; Chatonnet, A.; Lockridge, O. Evidence for a single butyrylcholinesterase gene in individuals carrying the C5 plasma cholinesterase variant (CHE2). FEBS. Lett., 1990, 262, 115-8.
9. Li, H.; Schopfer, L.L.; Masson, P.; Lockridge, O. Lamellipodin proline rich peptides associated with native plasma butyrylcholinesterase tetramers. Biochem. J., 2008, 411, 425-32.
10. Masson, P. A naturally occurring molecular form of human plasma cholinesterase is an albumin conjugate. Biochim. Biophys. Acta, 1989, 88, 258-66.
11. Lockridge, O.; Eckerson, H.W.; La Du, B.N. Interchain disulfide bonds and subunit organization in human serum cholinesterase. J. Biol. Chem., 1979, 254, 8324-30.
12. Altamirano, C.V.; Lockridge, O. Conserved aromatic residues of the C-terminus of human butyrylcholinesterase mediate the association of tetramers. Biochemistry, 1999, 38, 13414-22.
13. Lockridge, O.; Bartels, C.F.; Vaughan, T.A.; Wong, C.K.; Norton, S.E.; Johnson, L.L. Complete amino acid sequence of human serum cholinesterase. J. Biol. Chem., 1987, 262, 549-57.
14. Arpagaus, M.; Kott, M.; Vatsis, K.P.; Bartels, C.F.; LaDu, B.N.; Lockridge, O. Structure of the gene for human butyrylcholinesterase. Evidence for a single copy. Biochemistry, 1990, 29, 124-31.
15. Nachon, F.; Nicolet, Y.; Viguie, N.; Masson, P.; Fontecilla-Camp, J.C.; Lockridge, O. Engineering of a monomeric and lowglycosylated form of human butyrylcholinesterase: expression, purification, characterization and crystallization. Eur. J. Biochem., 2002, 269, 630-7.
16. Nicolet, Y.; Lockridge, O.; Masson, P.; Fontecilla-Camps, J.C.; Nachon, F. Crystal structure of human butyrylcholinesterase and of its complexes with substrate and products. J. Biol. Chem., 2003, 278, 41141-7.
17. Ngamelue, M.N.; Homma, K.; Lockridge, O.; Asojo, O.A. Crystallization and X-ray structure of full-length recombinant human butyrylcholinesterase. Acta Cryst. Sect F Struct. Biol. Cryst. Commun., 2007, 63, 723-7.
18. Saxena, A.; Redman, A.M.G.; Jiang, X.; Lockridge, O., Doctor, B.P. Differences in active site gorge dimensions of cholinesterases revealed by binding of inhibitors to human butyrylcholinesterase. Biochemistry, 1997, 36, 14642-51.
19. Viragh, C.; Harris, T.K.; Reddy, P.M.; Massiah, M.A.; Mildvan, A.S.; Kovach, I.M. NMR evidence for a short, strong hydrogen bond at the active site of a cholinesterase. Biochemistry, 2000, 26, 16200-5.
20. Tormos, J.R.; Wiley, K.L.; Seravalli, J.; Nachon, F.; Masson, P.; Nicolet, Y.; Quinn, D.M. The reactant state for substrate-activated turnover of acetylthiocholine by butyrylcholinesterase is a tetrahedral intermediate. J. Am. Chem. Soc., 2005, 127, 14538-9.
21. Masson, P.; Legrand, P.; Bartels, C.F.; Froment, M.T.; Schopfer, L.M.; Lockridge, O. Role of aspartate 70 and tryptophan 82 in binding of succinyldithiocholine to human butyrylcholinesterase. Biochemistry, 1997, 36, 2266-77.
22. Nachon, F.; Ehret-Sabatier, L.; Loew, D.; Colas, C.; van Dorsselaer, A.; Goeldner, M. Trp82 and Tyr332 are involved in two quaternary ammonium binding domains of human butyrylcholinesterase as revealed by photoaffinity labeling with [3H]DDF. Biochemistry, 1998, 37, 10507-13.
23. Nachon, F.; Asojo, O.A.; Borgstahl, G.E.; Masson, P.; Lockridge, O. Role of water in aging of human butyrylcholinesterase inhibited by echothiophate: the crystal structure suggests two alternative mechanisms of aging. Biochemistry, 2005, 44, 1154-62.
24. Carletti, E.; Li, H.; Ekstrom, F.; Nicolet, Y.; Loiodice, M.; Gillon, E.; Froment, M.T.; Lockridge, O.; Schopfer, L.M.; Masson, P.; Nachon, F. Aging of cholinesterases phosphylated by tabun proceeds through O-dealkylation. J. Am. Chem. Soc., 2008, 130(47) 16011-20.
25. Harel, M.; Sussman, J.L.; Krejci, E.; Bon ,S.; Chanal, P.; Massoulié, J.; Silman, I. Conversion of acetylcholinesterase to butyrylcholinesterase: modeling and mutagenesis. Proc Natl Acad Sci USA, 1992, 89, 10827-31.
26. Radic, Z.; Pickering, N.A.; Vellom, D.C.; Camp, S.; Taylor, P. Three distinct domains in the cholinesterase molecule confer selectivity for acetyl- and butyrylcholinesterase inhibitors. Biochemistry, 1993, 32, 12074-84.
27. Kaplan, D.; Ordentlich, A.; Barak, D.; Ariel, N.; Kronman, C.; Velan, B.; Shafferman, A. Does "butyrylization" of acetylcholinesterase through substitution of the six divergent aromatic amino acids in the active center gorge generate an enzyme mimic of butyrylcholinesterase? Biochemistry, 2001, 40, 7433-45.
28. Masson, P.; Froment, M.T.; Gillon, E.; Nachon, F.; Lockridge, O.; Schopfer, L.M. Hydrolysis of oxo- and thio-esters by human butyrylcholinesterase. Biochim. Biophys. Acta, 2007, 1774, 16-34.
29. Masson, P.; Froment, M.T.; Gillon, E.; Nachon, F.; Darvesh, S.; Schopfer, L.M. Kinetic analysis of butyrylcholinesterase-catalyzed hydrolysis of acetanilides. Biochim. Biophys. Acta, 2007, 1774, 1139-47.
30. Masson, P.; Adkins, S.; Gouet, P.; Lockridge, O. Recombinant human butyrylcholinesterase G390V, the fluoride-2 variant, expressed in Chinese hamster ovary cells, is a low affinity variant. J. Biol. Chem., 1993, 268, 14329-41.
31. Masson, P.; Froment, M.T.; Bartels, C.F.; Lockridge, O. Asp70 in the peripheral anionic site of human butyrylcholinesterase. Eur. J. Biochem., 1996, 235, 36-48.
32. Masson, P.; Xie, W.; Froment, M.T.; Levitsky, V.; Fortier, P.L.; Albaret, C.; Lockridge, O. Interaction between the peripheral site residues of human butyrylcholinesterase, D70 and Y332, in binding and hydrolysis of substrates. Biochim. Biophys. Acta, 1999, 1433, 281-93.
33. Masson, P.; Froment, M.T.; Bartels, C.F.; Lockridge, O. Importance of aspartate-70 in organophosphate inhibition, oxime reactivation and aging of human butyrylcholinesterase. Biochem. J., 1997, 325, 53-61.
34. Masson, P.; Froment, M.T.; Fortier, P.L.; Visicchio, J.E.; Bartels, C.F.; Lockridge, O. Butyrylcholinesterase-catalysed hydrolysis of aspirin, a negatively charged ester, and aspirin-related neutral esters. Biochim. Biophys. Acta, 1998, 1387, 41-52.
35. Masson, P.; Schopfer, L.M.; Froment, M.T.; Debouzy, J.C.; Nachon, F.; Gillon, E., Lockridge, O.; Hrabovska, A.; Goldstein, B.N. Hysteresis of butyrylcholinesterase in the approach to steady-state kinetics. Chem.-Biol. Interact., 2005, 157, 143-52.
36. Stojan, J.; Golicnik, G.; Froment, M.T.; Estour, F.; Masson, P. Concentration-dependent reversible activation-inhibition of human butyrylcholinesterase by tetraethylammonium ion. Eur. J. Biochem., 2002, 269, 1154-1161.
37. Masson, P.; Froment, M.T.; Gillon, E.; Nachon, F.; Lockridge, O. and Schopfer, L.M. Kinetic analysis of effector modulation of butyrylcholinesterase- catalysed hydrolysis of acetanilides and homologous esters., FEBS J., 2008, 275, 2617-2631.
38. Petroianu, G.A, Hasan, M.Y, Nurulain, S.M, Arafat, K.; Sheen, R.; Saleh, A.; Schmitt, A. Protective drugs in acute large-dose exposure to organophosphates: a comparison of metoclopramide and tiapride with pralidoxime in rats. Anesth Analg., 2005, 100, 382-386. (Pubitemid 40170529)
39. Petroianu, G.A.; Hasan, M.Y.; Arafat, K.; Nurulain, S.M.; Schmitt, A. Weak inhibitors protect cholinesterases from strong inhibitors (paraoxon): in vitro effect of tiapride. J. Appl. Toxicol., 2005, 25, 562-567. (Pubitemid 43041604)
40. Giacobini, E. 2003, Butyrylcholinesterase, its function and inhibitors, Martin Dunitz Pub.; London and New York x+181p.
41. Main, A.R. Mode of action of anticholinesterases. Pharmacol. Ther., 1979, 6, 579-628.
42. Gupta, R, (Ed). Toxicology of organophosphate and carbamate compounds. 2006, Elsevier Academic Press, San Diego, xv+763p.
43. Gupta, R, (Ed). Handbook of toxicology of chemical warfare agents, 2009, Elsevier Academic Press, San Diego, xviii+1147p.
44. Li, H.; Ricordel, I.; Tong, L.; Schopfer, L.M.; Baud, F.; Megabarne, B.; Maury, Masson, P. and Lockridge, O. Carbofuran poisoning detected by mass spectrometry of butyrylcholinesterase adduct in human serum. J. Appl. Toxicol., 2008, 29, 149-155.
45. Kamal, M.A.; Qu, X.; Yu, Q.S.; Tweedie, D.; Holloway, H.W.; Li, Y.; Tan, Y.; Greig, N.H. Tetrahydrofurobenzofuran cymserine, a potent butyrylcholinesterase inhibitor and experimental Alzheimer drug candidate, enzyme kinetic analysis. J. Neural. Transm., 2008, 115, 889-898.
46. Taylor, P.; Wong, L.; Radic, Z.; Tsilgeny, I.; Bruggeman, R.; Hosea, N.A. and Berman, H.A. Analysis of cholinesterase inactivation and reactivation by systematic structural modification and enantiomeric selectivity. Chem. Biol. Interact., 1999, 119-120, 3-15.
47. Bartling, A.; Worek, F.; Szinicz, L. and Thiermann, H. Enzymekinetic investigation of different sarin analogues reacting with human acetylcholinesterase and butyrylcholinesterase. Toxicol., 2007, 233, 166-172.
48. Worek, F.; Thiermann, H.; Szinicz, L.; Eyer, P. Kinetic analysis of interactions between human acetylcholinesterase, structurally different organophosphorus compounds and oximes. Biochem Pharmacol., 2004, 68, 2237-2248.
49. Worek, F.; Diepold, C.; Eyer, P. Dimethylphosphoryl-inhibited human cholinesterases: inhibition, reactivation, and aging kinetics. Arch Toxicol., 1999, 73, 7-14.
50. Michel, H.O.; Hackley, B.E.; Berkowitz, L.; List, G.; Hackley, E.B.; Gillilan, W. and Pankau, M. Ageing and dealkylation of Soman (pinacolylmethylphosphonofluoridate)-inactivated eel cholinesterase. Arch. Biochem. Biophys., 1967, 121, 29-34.
51. Li, H.; Schopfer, L.M.; Nachon, F.; Froment, M.T.; Masson, P and Lockridge, O. Aging pathways for organophosphate-inhibited human butyrylcholinesterase, including novel pathways for isomalathion, resolved by mass spectrometry. Toxicol. Sci., 2007, 100, 136-145.
52. Keijer, J.H.; Wolring, G.Z. Stereospecific aging of phosphonylated cholinesterases. Biochim. Biophys. Acta, 1969, 185, 465-468.
53. Masson, P.; Clery, C.; Guerra, P.; Redslob, A.; Albaret, C and Fortier, P.-L. 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., 1999, 343, 361-369.
54. Saxena, A.; Viragh, C.; Frazier, D.S.; Kovach, I.M.; Maxwell, D.M.; Lockridge, O.; Doctor, B.P. The pH dependence of dealkylation in soman-inhibited cholinesterases and their mutants: further evidence for a push-pull mechanism. Biochemistry, 1998, 37, 15086-15096.
55. Heilbronn, E. In vitro reactivation and "ageing" of Tabun inhibited blood cholinesterases; studies with N-methyl-pyridinium-2- aldoxime methane sulphonate and N,N'-trimethylene bis (pyridinium- 4-aldoxime) dibromide. Biochem. Pharmacol., 1963, 12, 25-36.
56. Sanson, B.; Nachon, Colletier, J.P.; Froment, M.T.; Toker, L.; Greenblatt, H.; Sussman, J.L.; Silman, I.; Masson, P.; Weik, M. Crystallographic snapshots of non-aged and aged conjugates of soman with acetylcholinesterase, and of a ternary complex of the aged conjugate with 2-PAM. J. Med. Chem., 2009, in press.
57. Darvesh, S.; Hopkin, D.A.; Geula, C. Neurobiology of butyrylcholinesterase. Nat. Rev. Neurosci., 2003, 4, 131-138.
58. 58] Girard, E.; Bernard, V.; Minic, J.; Chatonnet, A.; Krejci, E.; Molgo, J. Butyrylcholinesterase and the control of synaptic responses in acetylcholinesterase knockout mice. Life Sci., 2007, 80, 2380-2385.
59. Hartmann, J.; Kiewert, C.; Duysen, E.G.; Lockridge, O.; Greig, N.H.; Klein, J. Excessive hippocampal acetylcholine levels in acetylcholinesterase- deficient mice are moderated by butyrylcholinesterase activity. J. Neurochem., 2007, 100, 1421-1429.
60. Checler, F.; Grassi, J.; Vincent, J.P. Cholinesterases display genuine arylacylamidase activity but are totally devoid of intrinsic peptidase activities. J. Neurochem., 1994, 62, 756-763.
61. Inestrosa, N.C.; Dinamarca, M.C.; Alvarez, A. Amyloidcholinesterase interactions. Implications for Alzheimer's disease. FEBS. J., 2008, 275, 625-632.
62. Li, B.; Sedlacek, M.; Manoharan, I.; Boopathy, R.; Duysen, E.G.; Masson, P.; Lockridge, O. Butyrylcholinesterase, paraoxonase, and albumin esterase, but not carboxylesterase, are present in human plasma. Biochem. Pharmacol., 2005, 70, 1673-1684.
63. Inaba, T.; Stewart, D.J.; Kalow, W. Metabolism of cocaine in man. Clin. Pharmacol. Ther., 1978, 23, 547-552.
64. Hoffman, R.; Morasco, R.; Goldfrank, L. Administration of purified human plasma cholinesterase protects against cocaine toxicity in mice. J. Toxicol. Clin. Toxicol., 1996, 34, 259-266.
65. Lynch, T.; Mattes, C.; Singh, A.; Bradley, R.; Brady, R.; Dretchen, K. Cocaine detoxification by human plasma butyrylcholinesterase. Toxicol. Appl. Pharmacol., 1997, 145, 363-371.
66. Nigg, H.N.; Ramos, LE.; Graham, E.M.; Sterling, J.; Brown, S.; Cornell, J.A. Inhibition of human plasma and serum butyrylcholinesterase (EC 3.1.1.8) by alpha-chaconine and alpha-solanine. Fundam. Appl. Toxicol., 1996, 33, 272-281.
67. Masson, P.; Nachon, F.; Broomfield, C.A.; Lenz, D.E.; Verdier, L.; Schopfer, L.M.; Lockridge, O. A collaborative endeavor to design cholinesterase-based catalytic scavengers against toxic organophosphorus esters. Chem. Biol. Interact., 2008, 175, 273-280.
68. Ostergaard, D.; Viby-Mogensen, J.; Rasmussen, S.N.; Gatke, M.R.; Varin, F. Pharmacokinetics and pharmacodynamics of mivacurium in patients phenotypically homozygous for the atypical plasma cholinesterase variant: effect of injection of human cholinesterase. Anesthesiology, 2005, 102, 1124-1132.
69. Ashani, Y. Prospective of human butyrylcholinesterase as a detoxifying antidote and potential regulator of controlled-release drugs. Drug. Dev. Res. 2000, 50, 298-308.
70. Ashani, Y.; Pistinner, S. Estimation of the upper limit of human butyrylcholinesterase dose required for protection against organophosphates toxicity: a mathematically based toxicokinetic model. Toxicol. Sci., 2004, 77, 358-367.
71. Mattes, C.E.; Lynch, T.J.; Singh, A.; Bradley, R.M.; Kellaris, P.A.; Brady, R.O.; Dretchen, K.L. Therapeutic use of butyrylcholinesterase for cocaine intoxication. Toxicol. Appl. Pharmacol. 1997, 145, 372-380.
72. Xie W.; Altamirano, CV.; Bartels, C.F.; Speirs, R.J.; Cashman, J.R.; Lockridge, O. An improved cocaine hydrolase: the A328Y mutant of human butyrylcholinesterase is 4-fold more efficient. Mol. Pharmacol., 1999, 55, 83-91.
73. Sun, H.; Pang, Y.P.; Lockridge, O.; Brimijoin, S. Re-engineering butyrylcholinesterase as a cocaine hydrolase. Mol. Pharmacol., 2002, 62, 220-224.
74. Pancook, J.D.; Pecht, G.; Ader, M.; Lockridge, O. ;Watkins, J.D. Application of directed evolution technology to optimize the cocaine hydrolase activity of human butyrylcholinesterase. FASEB J., 2003, 17, A565.
75. Pan, Y.; Gao, D.; Yang, W.; Cho, H.; Yang G, Tai, H.; Zhan, C.G. Computational redesign of human butyrylcholinesterase for anticocaine medication. Proc. Natl. Acad. Sci. USA, 2005, 102, 16656-16661.
76. Zheng, F.; Zhang, C.G. Structure-and-mechanism-based design and discovery of therapeutics for cocaine overdose and addiction. Org. Biomol. Chem., 2008, 6, 836-843.
77. Brimijoin, S.; Gao, Y.; Anker, J.; Gliddon, L.A.; LaFleur, D.; Shah, R.; Zhao, Q.; Singh, M.; Carroll, M.E. A cocaine hydrolase engineered from human butyrylcholinesterase selectively blocks cocaine toxicity and reinstatement of drug seeking in rats. Neuropsychopharmacol., 2008, 33, 2715-2725.
78. Saxena, A.; Luo, C.; Chilukuri, N.; Maxwell, D.M.; Doctor, B.P. Novel approaches to medical protection against chemical warfare nerve agents. In Chemical Warfare Agents: Chemistry, Pharmacology, Toxicology and Therapeutics; Romano, J.A.; Luckey, B.J.; Salem, H., Eds; CRC Press: Boca Raton, Fl, 2007, pp. 145-173.
79. Lenz, D.E.; Broomfield, C.A.; Yeung, D.T.; Masson, P.; Maxwell, D.M.; Cerasoli, D.M. Nerve agent bioscavengers: progress in development of a new mode of protection against organophosphorus exposure. In Chemical Warfare Agents: Chemistry, Pharmacology, Toxicology and Therapeutics; Romano, J.A.; Luckey, B.J.; Salem, H., Eds; CRC Press: Boca Raton, Fl, 2007; pp. 175-202.
80. Jäarv, J. Insight into the putative mechanism of esterase acting simultaneously on carboxyl and phosphoryl compounds. In Enzymes hydrolyzing organophosphorus compounds. Reiner, E.; Aldridge, W.N.; Hoskin, F.C.G., Eds; Ellis Horwood Ldt Pub.: Chichester, UK, 1989, pp. 221-225.
81. Millard, C.B.; Lockridge, O.; Broomfield, C.A. Design and expression of organophosphorus acid anhydride hydrolase activity in human butyrylcholinesterase. Biochemistry, 1995, 34, 15925-15933.
82. Lockridge, O.; Blong, R.M.; Masson, P.; Froment, M.T.; Millard, C.B.; Broomfield, C.A. A single amino acid substitution, Gly117His, confers phosphotriesterase (organophosphorus acid anhydride hydrolase) activity on human butyrylcholinesterase. Biochemistry, 1997, 36, 786-795.
83. Millard, C.B.; Lockridge, O.; Broomfield, C.A. Organophosphorus acid anhydride hydrolase activity in human butyrylcholinesterase: synergy results in a somanase. Biochemistry, 1998, 37, 237-247.
84. Albaret, C.; Masson, P.; Broomfield, C.A.; El Kaim, L.; Fortier, P.L. Mechanical aspects of the phosphotriesterase activity of human butyrylcholinesterase G117H mutant. In Structure and function of cholinesterases and related proteins; Doctor, B.P; Quinn, D.M.; Taylot, P.; Rotundo, R.L., Eds.; Plenum Press: New York, 1998, pp. 399-405.
85. Lockridge, O.; Schopfer, L.M.; Winger, G.; Woods, J.H. Large scale purification of butyrylcholinesterase from human plasma suitable for injection into monkeys; a potential new therapeutic for protection against cocaine and nerve agent toxicity. J. Med. Chem. Biol. Radiol. Def., 2005, 3-nihms5095.
86. Soreq, H.; Seidman, S.; Dreyfus, P.A.; Zevin-Sonkin, D.; Zakut, H. Expression and tissue-specific assembly of human butyrylcholine esterase in microinjected Xenopus laevis oocytes. J. Biol. Chem. 1989, 264, 10608-10613.
87. Masson P. Expression and refolding of functional human butrylcholinesterase from E. coli. In Multiple approaches to cholinesterase functions, Shafferman, A.; Velan, B., Eds.; Plenum: New York, 1993, pp. 49-52.
88. Kris, M.; Jbilo, O.; Bartels, C.F.; Masson, P.; Rhode, S.; Lockridge, O. Endogenous butyrylcholinesterase in SV40 transformed cell lines: COS-1, COS-7, MRC-5 SV40, and WI-38 VA13. In vitro Cell. Dev. Biol., 1994, 30A, 680-689.
89. Duysen, E.G.; Bartels, C.F.; Lockridge, O. Wild-type and A328W mutant human butyrylcholinesterase tetramers expressed in Chinese hamster ovary cells have a 16-hour half-life in the circulation and protect mice from cocaine toxicity. J. Pharmacol. Exp. Ther., 2002, 302, 751-758.
90. Platteborze, P.L.; Broomfield, C.A. Expression of biologically active human butyrylcholinesterase in the cabbage looper (Trichoplusia ni). Biotechnol. Appl. Biochem., 2000, 31, 225-229.
91. Wei, W.L.; Qin, J.C. ; Sun, M.J. High-level expression of human butyrylcholinesterase gene in Bombyx mori and biochemicalpharmacological characteristic study of its product. Biochem. Pharmacol., 2000, 60, 121-126.
92. Huang,Y.J, HuangY.; Baldassarre, H.; Wang, B.; Lazaris, A.; Leduc, M.; Bilodeau, A.S.; Bellemare, A.; Côté, M.; Herskovits, P.; Touati, M.; Turcotte, C.; Valeanu, L.; Lemée, N.; Wilgus, H.; Bégin, I.; Bhatia, B.; Rao, K.; Neveu, N.; Brochu, E.; Pierson, J.; Hockley, D.K.; Cerasoli, D.M.; Lenz, D.E.; Karatzas, C.N.; Langermann, S. Recombinant human butyrylcholinesterase from milk of transgenic animals to protect against organophosphate poisoning. Proc. Natl. Acad. Sci. USA, 2007, 104, 13603-13608.
93. Chilukuri, N.; Sun, W.; Naik, R.S.; Parikh, K.; Tang, L.; Doctor. B.P.; Saxena, A. Effect of polyethylene glycol modification on the circulatory stability and immunogenicity of recombinant human butyrylcholinesterase. Chem. Biol. Interact., 2008, 175, 255-260.
94. Huang, Y.J.; Lundy, P.M.; Lazaris,A.; Huang, Y.; Baldassarre, H.; Wang, B.; Turcotte, C.; Cote, M.; Bellemare, A.; Bilodeau, A.S.; Brouillard, S.; Touati, M.; Herskovits, P.; Begin, I.; Neveu, N.; Brochu, E.; Pierson, J.; Hockley, D.K.; Cerasoli, D.M.; Lenz, D.E.; Wilgus, H.; Karatzas, C.N.; Langermann, S. Substantially improved pharmacokinetics of recombinant human butyrylcholinesterase by fusion to human serum albumin. BMC Biotechnol., 2008, 8, 50.
95. Chilukuri, N.; Duysen, E.G.; Parikh, K.; Sun, W.; Doctor, B.P.; Lockridge, O.; Saxena, A. Adenovirus-mediated gene transfer of human butyrylcholinesterase results in persistent high-level transgene expression in vivo. Chem. Biol. Interact., 2008, 175, 327-331.
96. Imato, T.; Ishibashi, N. Potentiometric butyrylcholine sensor for organophosphate pesticides. Biosens. Bioelectron., 1995, 10, 435-441.
97. Cho, Y.A.; Lee, H.S.; Cha, G.S.; Lee, Y.T. Fabrication of butyrylcholinesterase sensor using polyurethane-based ion-selective membranes. Biosens. Biolectron., 1999, 14, 435-438.
98. Campanella, L.; Cocco, R.; Favero, G.; Sammartino, M.P.; Tomassetti, M. Eptastigmine, nicotinamide and nicotinic acid determination using an inhibition enzyme sensor; application to pharmaceutical analysis. Ann. Chim., 2002, 92, 373-385.
99. Mitsubayashi, K.; Nakayama, K.; Taniguchi, M.; Saito, H.; Otsuka, K.; Kudo, H. Bioelectronic sniffer for nicotine using enzyme inhibition. Anal. Chim. Acta, 2006, 573, 69-74.
100. Korpan, Y.I.; Raushel, F.M.; Nazarenko, E.A.; Soldatkin, A.P.; Jaffrezic-Renault, N.; Martelet, C. Sensitivity and specificity improvement of an ion sensitive field effect transistors-based biosensor for potato glycoalkaloids detection. J. Agric. Food. Chem., 2006, 54, 707-712.
101. Luckarift, H.R.; Greenwald, R.; Bergin, M.H.; Spain, J.C.; Johnson, G.R. Biosensor system for continuous monitoring of organophosphate aerosols. Biosens. Bioelectron., 2007, 23, 400-406.
102. Arduini, F.; Amine, A.; Moscone, D.; Ricci, F.; Palleschi, G. Fast, sensitive and cost-effective detection of nerve agents in the gas phase using a portable instrument and an electrochemical biosensor. Anal. Bioanal. Chem., 2007, 388, 1049-1057.