Why has butyrylcholinesterase been retained? Structural and functional diversification in a duplicated gene

Neurochemistry International

Volumn 61, Issue 5, 2012, Pages 783-797

  Johnson, Glynis ^a   Moore, Samuel W ^a  

^a UNIVERSITY OF STELLENBOSCH   (South Africa)

Author keywords

Acetylcholinesterase; Butyrylcholinesterase; Detoxification; Evolution; Mutation; Subfunctionalisation

Indexed keywords

ACETYLCHOLINESTERASE; CHOLINESTERASE; CHOLINESTERASE INHIBITOR; DONEPEZIL; GALANTAMINE; HUPERZINE A; ISO OMPA; PHYSOSTIGMINE;

ALZHEIMER DISEASE; BIOMPHALARIA GLABRATA; CATALYSIS; DETOXIFICATION; ENZYME STRUCTURE; GENE DUPLICATION; GENE FUNCTION; GENE MUTATION; HUMAN; INFORMATION RETRIEVAL; KNOCKOUT MOUSE; MUTATION; NEUROMUSCULAR SYNAPSE; NEUROTRANSMISSION; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROCAMBARUS CLARKII; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PUBLISHING; REVIEW;

ANIMALIA; VERTEBRATA;

EID: 84866511477     PISSN: 01970186     EISSN: 18729754     Source Type: Journal    
DOI: 10.1016/j.neuint.2012.06.016     Document Type: Short Survey

References (220)

1. C.A. Abbott, M.I. Mackress, S. Kumar, A.O. Olukoga, C. Gordon, S. Arrol, D. Bhatnager, A.J. Boulton, and P.N. Durrington Relationship between serum butyrylcholinesterase activity, hypertriglyceridaemia and insulin sensitivity in diabetes mellitus Clin. Sci. 85 1993 77 81
2. M.B. Abou-Donia, W.A. Khan, A.M. Dechkovskaia, L.B. Goldstein, S.L. Bullman, and A. Abdel-Rahman In utero exposure to nicotine and chlorpyrifos alone, and in combination produces persistent sensorimotor deficits and Purkinje neuron loss in the cerebellum of adult offspring rats Arch. Toxicol. 80 2006 620 631
3. R.A. Acey, S. Bailey, P. Healy, C. Jo, T.F. Unger, and R.A. Hudson Butyrylcholinesterase in the early development of the brine shrimp (Artemia salina) larvae: a target for phthalate ester embryotoxicity? Biochem. Biophys. Res. Commun. 299 2002 659 662
4. M. Acuňa, L. Eaton, N.R. Ramirez, L. Cifuentes, and E. Llop Genetic variants of serum butyrylcholinesterase in Chilean Mapuche Indians Am. J. Phys. Anthropol. 121 2003 81 85
5. M. Adler, H.A. Manley, A.L. Purcell, S.S. Deshpande, T.A. Hamiton, R.K. Kan, G. Oyler, O. Lockridge, E.G. Duysen, and R.E. Sheridan Reduced acetylcholine receptor density, morphological remodeling and butyrylcholinesterase activity can sustain muscle function in acetylcholinesterase knockout mice Muscle Nerve 30 2004 317 327
6. V.N. Akhypova, S.V. Dzyadevych, A.P. Soldatkin, A.V. El'skaya, C. Martelet, and N. Jaffrezic-Renault Development and optimisation of biosensors based on pH-sensitive field effect transistors and cholinesterases for sensitive detection of solanaceous glycoalkaloids Biosens. Bioelectron. 18 2003 1047 1053
7. M.C. Alavanja, and M.R. Bonner Occupational pesticide exposures and cancer risk: a review J. Toxicol. Environ. Health B Crit. Rev. 15 2012 238 263
8. V.M. Alcântara, M.A. De Lourenço, F.M. Slazano, M.L. Petzl-Erler, C.E. Coimbra Jr., R.V. Santos, and E.A. Chautard-Freire-Maia Butyrylcholinesterase polymorphisms (BCHE and CHE5 loci) in Brazilian Indian and admixed populations Hum. Biol. 67 1995 717 726
9. V.M. Alcântara, E.A. Chautard-Freire-Maia, M. Scartezini, M.S. Cerci, K. Braun-Prado, and G. Picheth Butyrylcholinesterase activity and risk factors for coronary artery disease Scand. J. Clin. Lab. Invest. 62 2002 399 404
10. N. Allon, L. Raveh, E. Gilat, E. Cohen, J. Grunwald, and Y. Ashani Prophylaxis against soman inhalation toxicity in guinea pigs by pretreatment alone with human serum butyrylcholinesterase Toxicol. Sci. 43 1998 121 128
11. C.V. Altamirano, C.F. Bartels, and O. Lockridge The butyrylcholinesterase K-variant shows similar cellular protein turnover and quaternary interaction to the wild-type enzyme J. Neurochem. 74 2000 869 877
12. M.G. Aluigi, C. Angolini, C. Falugi, R. Fossa, P. Genever, L. Gallus, P.G. Layer, G. Prestipino, Z. Raconczay, M. Sgro, H. Thielecke, and S. Trombino Interaction between organophosphate compounds and cholinergic functions during development Chem. Biol. Interact. 157-158 2005 305 316
13. R. Alvarez, M.P. Honrubia, and M.P. Herráez Skeletal malformations induced by the insecticides 22-Aphox and Folidol during larval development of Rana perezi Arch. Environ. Contam. Toxicol. 28 1995 349 356
14. J. Antosiewicz, S.T. Wlodek, and J.A. McCammon Acetylcholinesterase: role of the enzyme's charge distribution in steering charged ligands toward the active site Biopolymers 39 1996 85 94
15. Y. Ashani, S. Shapira, D. Levy, A.D. Wolfe, B.P. Doctor, and L. Raveh Butyrylcholinesterase and acetylcholinesterase prophylaxis against soman poisoning in mice Biochem. Pharmacol. 41 1991 37 41
16. D.S. Auld, and R. Robitaille Glial cells and neurotransmission: an inclusive view of synaptic function Neuron 40 2003 89 400
17. C.G. Ballard, N.H. Greig, A.L. Guillozer-Bongaarts, A. Enz, and S. Darvesh Cholinesterases: roles in the brain during health and disease Curr. Alzheimer Res. 2 2005 307 318
18. C.F. Bartels, F.S. Jensen, O. Lockridge, A.F. van der Spek, H.M. Rubinstein, T. Lubrano, and B.N. La Du mutation associated with the human butyrylcholinesterase K-variant and its linkage to the atypical variant mutation and other polymorphic sites Am. J. Hum. Genet. 50 1992 1086 1103
19. M. Behra, X. Cousin, C. Bertrand, J.L. Vanesch, D. Biellmann, A. Chatonnet, and U. Strähle Acetylcholinesterase is required for neuronal and muscular development in the zebrafish embryo Nat. Neurosci. 5 2002 111 118
20. E. Ben-Assayag, S. Shenhar-Tsarfaty, K. Ofek, L. Soreq, I. Bova, L. Shopin, R.M. Berg, S. Berliner, I. Shapira, N.M. Bornstein, and H. Soreq Serum cholinesterase activities distinguish between stroke patients and controls and predict 12-month mortality Mol. Med. 16 2010 278 286
21. O. Ben Menachem-Zidon, A. Avital, Y. Ben-Menahem, I. Goshen, T. Kreisel, E.M. Schmueli, M. Segal, T. Ben Hur, and R. Yirmiya Astrocytes support hippocampal-dependent memory and long-term potentiation via interleukin-1 signaling Brain Behav. Immun. 25 2011 1008 1016
22. B. Benyamin, R.P. Middelburg, P.A. Lind, A.M. Valle, S. Gordon, D.R. Nyholt, S.E. Medland, A.K. Henders, A.C. Heath, P.A. Madden, P.M. Visscher, D. O'Connor, G.W. Montgomery, N.G. Martin, and J.B. Whitfield GWAS of butyrylcholinesterase activity identifies four novel loci, independent effects with BChE and secondary associations with metabolic risk factors Hum. Mol. Genet. 20 2011 4504 4514
23. C.C. Bernardi, S. Ribeiro Ede, I.J. Cavalli, E.A. Chautard-Freire-Maia, and R.L. Souza Amplification and deletion of the acetylcholinesterase and butyrylcholinesterase cholinesterase genes in sporadic breast cancer Cancer Genet. Cytogenet. 197 2010 158 165
24. C. Bertrand, A. Chatonnet, C. Takke, Y.L. Yan, J. Postlethwait, J.-P. Toutant, and X. Cousin Zebrafish acetylcholinesterase is encoded by a single gene localized on linkage group 7. Gene structure and polymorphism: molecular forms and expression pattern during development J. Biol. Chem. 276 2001 464 474
25. B. Blondet, G. Carpentier, A. Ferry, A. Chatonnet, and J. Courty Localization of butyrylcholinesterase at the neuromuscular junction of normal and acetylcholinesterase knockout mice J. Histochem. Cytochem. 58 2010 1075 1082
26. E. Bodur, and A.N. Cokugras The effects of indole-3-acetic acid on human and horse serum butyrylcholinesterase Chem. Biol. Interact. 157-158 2005 375 378
27. E. Bodur, and P.G. Layer Counter-regulation of cholinesterases: differential activation of PKC and ERK signaling in retinal cells through butyrylcholinesterase knockdown Biochimie 93 2011 469 476
28. S.A. Botti, C.E. Felder, J.L. Sussman, and I. Silman Electrotactins: a class of adhesion proteins with conserved electrostatic and structural motifs Protein Eng. 11 1998 415 420
29. S. Brimijoin, and P. Hammond Butyrylcholinesterase in human brain and acetylcholinesterase in human plasma: trace enzymes measured by two-site immunoassay J. Neurochem. 51 1988 1227 1231
30. C.A. Broomfield, D.M. Maxwell, R.P. Solana, C.A. Castro, A.V. Finger, and D.E. Lenz Protection by butyrylcholinesterase against orgnaophosphate poisoning in nonhuman primates J. Pharmacol. Exp. Ther. 259 1991 633 638
31. R. Bullock, and R. Lane Executive dyscontrol in dementia, with emphasis on subcortical pathology and the role of butyrylcholinesterase Curr. Alzheimer Res. 4 2007 277 293
32. G. Carmignato, and P.G. Haydon Astrocyte calcium signaling and epilepsy Glia 2012 10.1002/glia.22318
33. F. Cerbai, M.G. Giovanini, C. Melani, A. Enz, and G. Pepeu N1phenethyl-norcymserine, a selective butyrylcholinesterase inhibitor, increases acetylcholine release in rat cerebral cortex: a comparison with donepezil and rivastigmine Eur. J. Pharmacol. 572 2007 142 150
34. A. Chatonnet, and O. Lockridge Comparison of butyrylcholinesterase and acetylcholinesterase Biochem. J. 260 1989 625 634
35. F. Checler, J. Grassi, and J.-P. Vincent Cholinesterases display genuine arylacylamidase activity but are totally devoid of intrinsic peptidase activities J. Neurochem. 62 1994 756 763
36. V.P. Chen, H.Q. Xie, W.K. Chan, K.W. Leung, G.K. Chan, R.C. Choi, S. Bon, J. Massouliè, and K.W. Tsim The PRiMA-linked cholinesterase tetramers are assembled from homodimers: hybrid molecules composed of acetylcholinesterase and butyrylcholinesterase dimers are up-regulated during development of chicken brain J. Biol. Chem. 285 2010 27265 27278
37. L.L. Colgin, D. Kubota, and G. Lynch Cholinergic plasticity in the hippocampus Proc. Natl. Acad. Sci. USA 100 2003 2872 2877
38. D. Combes, Y. Fedon, M. Grauso, J.-P. Toutant, and M. Arpagaus Four genes encode acetylcholinesterases in the nematodes Caenorhabditis elegans and Caenorhabditis briggsae. cDNA sequences, genomic structures, mutations and in vivo expression J. Mol. Biol. 300 2000 727 742
39. E.H. Corder, A.M. Saunders, W.J. Strittmatter, D.E. Schmechel, P.C. Gaskell, G.W. Small, A.D. Roses, J.L. Haines, and M.A. Pericak-Vance Gene dose of apolipoprotein E type 4 allele and the risk of Alzheimer's disease in late onset families Science 261 1993 921 923
40. V. Coronas, M. Durand, J.G. Chabot, F. Jourdan, and R. Quirion Acetylcholine induces neuritic outgrowth in rat primary olfactory bulb cultures Neuroscience 98 2000 213 219
41. B. Czèh, and B. Di Benedetto Antidepressants act directly on astrocytes: evidences and functional consequences Eur. Neuropsychopharmacol. 2012 http://dx.doi.org/10.1016/j.euroneuro.2012.04.017
42. T. Darreh-Shori, N. Modiri, K. Blennow, S. Baza, C. Kamil, H. Ahmed, N. Andreasen, and A. Nordberg The apolipoprotein E 4 allele plays pathological roles in AD through high protein expression and interaction with butyrylcholinesterase Neurobiol. Aging 32 2011 1236 1248
43. S. Darvesh, D.L. Grantham, and D.A. Hopkins Differentiation of butyrylcholinesterase in the human amygdala and hippocampal formation J. Comp. Neurol. 393 1998 374 390
44. S. Darvesh, S.E. MacDonald, A.M. Losier, E. Martin, D.A. Hopkins, and J.A. Armour Cholinesterases in cardiac ganglia and modulation of canine intrinsic cardiac neuronal activity J. Auton. Nerv. Syst. 71 1998 75 84
45. S. Darvesh, R. Kumar, S. Roberts, R. Walsh, and E. Martin Butyrylcholinesterase-mediated enhancement of the enzymatic activity of trypsin Cell. Mol. Neurobiol. 21 2001 285 296
46. S. Darvesh, and D.A. Hopkins Differential distribution of butyrylcholinesterase and acetylcholinesterase in the human thalamus J. Comp. Neurol. 463 2003 25 43
47. U.N. Das Acetylcholinesterase and butyrylcholinesterase as possible markers of low-grade systemic inflammation Med. Sci. Monit. 13 2007
48. T. DeVos, and T.A. Dick Characterization of cholinesterases from the parasitic nematode Trichinella spiralis Comp. Biochem. Physiol. C Toxicol. Pharmacol. 103 1992 129 134
49. D. De Vriese, F. Gregoire, R. Lema-Kisoka, M. Waelbroeck, P. Robberecht, and C. Delporte Ghrelin degradation by serum and tissue homogenates: identification of the cleavage sites Endocrinology 145 2004 4997 5005
50. D.C. Dey, M. Maekawa, K. Sudo, and T. Kanno Butyrylcholinesterase genes in individuals with abnormal inhibition numbers and with trace activity: one common mutation and two novel silent genes Ann. Clin. Biochem. 35 1998 302 310
51. U. Drews Cholinesterases in embryonic development Prog. Histochem. Cytochem. 7 1975 1 52
52. E.G. Duysen, B. Li, W. Xie, L.M. Schopfer, R.S. Anderson, C.A. Broomfield, and O. Lockridge Evidence for non-acetylcholinesterase targets of organophosphorus nerve agents: supersensitivity of the acetylcholinesterase knockout mouse to VX lethality J. Pharmacol. Exp. Ther. 299 2001 528 535
53. E.G. Duysen, S. Darvesh, and O. Lockridge Sensitivity of butyrylcholinesterase knockout mice to (-)-huperzineA and donepezil suggests humans with butyrylcholinesterase deficiency may not tolerate these Alzheimer's disease drugs and indicates butyrylcholinesterase function in neurotransmission Toxicology 233 2007 60 69
54. E.G. Duysen, B. Li, and O. Lockridge The butyrylcholinesterase knockout mouse: a research tool in the study of drug sensitivity, bio-distribution, obesity and Alzheimer's disease Expert Opin. Drug Metab. Toxicol. 5 2009 523 528
55. G. Ehrlich, D. Ginzberg, Y. Loewenstein, D. Glick, B. Kerem, S. Ben-Ari, H. Zakut, and H. Soreq Population diversity and distinct haplotype frequencies associated with ACHE and BCHE genes of Israeli Jews from trans-Caucasian Georgia and from Europe Genomics 22 1994 288 295
56. M. En-Nosse, S. Hartmann, K. Trinkaus, V. Alt, B. Stigler, C. Heiss, O. Kilian, R. Schnettler, and K.S. Lips Expression of non-neuronal cholinergic system in osteoblast-like cells and its involvement in osteogenesis Cell Tissue Res. 338 2009 203 215
57. R.I. Erickson, A.A. Paucar, R.L. Jackson, K. Visnyei, and H. Kornblum Roles of insulin and transferrin in neural progenitor survival and proliferation J. Neurosci. Res. 86 2008 1884 1894
58. J. Espallargues, L. Galvan, F. Sabatier, V. Rana-Poussine, T. Maurice, and A. Chatonnet Behavioural phenotyping of heterozygous acetylcholinesterase knockout (ACHE +/-) mice showed no memory enhancement but hypersensitivity to amnesic drugs Behav. Brain Res. 206 2010 263 273
59. R.T. Evans, and J. Wardell On the identification and frequency of the J and K cholinesterase phenotypes in a Caucasian population J. Med. Genet. 21 1984 99 102
60. P.R. Flood Histochemistry of cholinesterase in amphioxus (Branchiostoma lanceolatum; Pallas) J. Comp. Neurol. 157 1974 407 437
61. S.E. Fontoura-da-Silva, and E.A. Chautard-Freire-Maia Butyrylcholinesterase variants (BCHE and CHE2 loci) associated with erythrocyte acetylcholinesterase inhibition in farmers exposed to pesticides Hum. Hered. 46 1996 142 147
62. A. Force, M. Lynch, F.B. Pickett, A. Amores, Y.L. Yan, and J. Postlethwait Preservation of duplicate genes by complementary, degenerative mutations Genetics 151 1999 1531 1545
63. A. Friedman, D. Kaufer, J. Shemer, I. Hendler, H. Soreq, and I. Tur-Kaspa Pyridostigmine brain penetration under stress enhances neuronal excitability and induces early immediate transcriptional response Nat. Med. 2 1996 1382 1385
64. Y. Furukawa-Hibi, T. Alkam, A. Nitta, A. Matsutama, H. Mizoguchi, K. Suzuki, S. Moussaoui, Q.S. Yu, N.H. Greig, T. Nagai, and K. Yamada Butyrylcholinesterase inhibitors ameliorate cognitive dysfunction induces by amyloid-β peptide in mice Behav. Brain Res. 225 2011 222 229
65. M.R. Gatke, J.R. Bundgaard, and J. Viby-Mogensen Two novel mutations in the BCHE gene in patients with prolonged duration of action of mivacurium or succinylcholine during anaesthesia Pharmacogenet. Genomics 17 2007 995 999
66. J. Ghedira, J. Jebali, Z. Bouraoui, M. Banni, L. Chouba, and M. Boussetta Acute effects of chlorpyrifos-ethyl and secondary treated effluents on acetylcholinesterase and butyrylcholinesterase activities in Carcinus maenas J. Environ. Sci. 21 2009 1467 1472
67. E. Giacobini Selective inhibitors of butyrylcholinesterase: a valid alternative for therapy for Alzheimer's disease? Drugs Aging 18 2001 891 898
68. E. Giacobini, P.L. Griffini, and T. Maggi The effect of MF8622, a selective butyrylcholinesterase inhibitor, on cortical levels of acetylcholine Soc. Neurosci. 22 2003 203
69. M.M. Gilbert, and V.J. Auld Evolution of clams (cholinesterase-like adhesion molecules): structure and function during development Front. Biosci. 10 2005 2177 2192
70. E. Girard, V. Bernard, J. Minic, A. Chatonnet, E. Krejci, and J. Molgó Butyrylcholinesterase and the control of synaptic responses in acetylcholinesterase knockout mice Life Sci. 80 2007 2380 2385
71. P. Glynn NTE: one target protein for different toxic mechanisms? Bioessays 25 2003 742 745
72. P. Gómez-Ramos, and M.A. Morán Ultrastructural localization of butyrylcholinesterse in senile plaques in the brains of aged and Alzheimer's disease patients Mol. Chem. Neuropathol. 30 1997 161 173
73. A.M. Graybiel, and C.W. Ragsdale Pseudocholinesterase staining in the primary visual pathway of the macaque monkey Nature 299 1982 439 442
74. N.H. Greig, T. Utsuki, D.K. Ingram, Y. Wang, G. Pepeu, C. Scali, Q.S. Yu, J. Mamczarz, H.W. Holloway, T. Giordano, D. Chen, K. Furukawa, K. Sambamurti, A. Brossi, and D.K. Lahiri Selective butyrylcholinesterase inhibition elevates brain acetylcholine, augments learning and lowers Alzheimer beta-peptide in rodent Proc. Natl. Acad. Sci. USA 102 2005 17213 17218
75. M. Harel, L.K. Sonosa, I. Silman, J.L. Sussman, and T.L. Rosenberry The crystal structure of thioflavin T bound to the peripheral site of Torpedo californica acetylcholinesterase reveals how thioflavin acts as a sensitive fluorescent reporter of ligand binding to the acylation site J. Am. Chem. Soc. 130 2008 7856 7861
76. M. Harris, and M. Whittaker Differential inhibition of the serum cholinesterase phenotypes by solanine and soladine Ann. Hum. Genet. 26 1962 73 76
77. Y. Hasin, N. Avidan, D. Bercovich, A. Kovczyn, I. Silman, J.S. Beckman, and J.L. Sussman A paradigm for single nucleotide polymorphism analysis: the case of the ACHE gene Hum. Mutat. 24 2004 408 416
78. J.E. Haux, O. Lockridge, and J.E. Casida Specificity of ethephon as a butyrylcholinesterase inhibitor and phosphorylating agent Chem. Res. Toxicol. 15 2002 1527 1533
79. S.B. Hedges Molecular evidence for the early history of living vertebrates P.E. Ahlberg, Major Events in Early Vertebrate Evolution: Palaeontology, Phylogeny, Genetics and Development 2001 Taylor and Francis London 119 134
80. C.T. Hittinger, and S.B. Carroll Gene duplication and the adaptive evolution of a classic genetic switch Nature 449 2007 677 681
81. M. Holmquist Alpha/beta-hydrolase fold enzymes: structures, functions and mechanisms Curr. Protein Pept. Sci. 1 2000 209 235
82. N.A. Hosea, Z. Radic, I. Tsigelny, H.A. Berman, D.M. Quinn, and P. Taylor Aspartate 74 as a primary determinant in acetylcholinesterase governing specificity to cationic organophosphates Biochemistry 35 1996 10995 11004
83. N.C. Inestrosa, M.C. Dinamarca, and A. Alvarez Amyloid-cholinesterase interactions. Implications for Alzheimer's disease FEBS J. 275 2008 625 632
84. T. Iwasaki, M. Yoneda, N. Nakajima, and Y. Terauchi Serum butyrylcholinesterase is strongly associated with adiposity, the serum lipid profile and insulin resistance Intern. Med. 46 2007 1633 1639
85. O. Jbilo, C.F. Bartels, A. Chatonnet, J.-P. Toutant, and O. Lockridge Tissue distribution of human acetylcholinesterase and butyrylcholinesterase messenger RNA Toxicon 32 1994 1445 1457
86. H. Jiang, and X.J. Zhang Acetylcholinesterase and apoptosis. A novel perspective for an old enzyme FEBS J. 275 2008 612 617
87. G. Johnson, and S.W. Moore The carboxylesterase/cholinesterase gene family in invertebrate deuterostomes Comp. Biochem. Physiol. D Genomics Proteomics 7 2012 83 93
88. G. Johnson, C. Swart, and S.W. Moore Interaction of acetylcholinesterase with the G4 domain of the laminin alpha1 chain Biochem. J. 411 2008 509 514
89. J. Kálmán, A. Juhász, Z. Rakonczay, G. Abrahám, M. Zana, K. Boda, T. Farkas, B. Penke, and Z. Janka Increased serum butyrylcholinesterase activity in type IIb hyperlipidaemic patients Life Sci. 75 2004 1195 1204
90. W. Kalow, and N. Staron On distribution and inheritance of atypical forms of human serum cholinesterase indicated by dibucaine numbers Can. J. Biochem. Physiol. 35 1957 1305 1320
91. D. Kaplan, A. Ordentlich, D. Barak, N. Ariel, C. Kronman, B. Velan, and A. Shafferman Does "butyrylization" of acetylcholinesterase through subsitution of the six divergent aromatic amino acids in the active center gorge generate an enzyme mimic of butyrylcholinesterase? Biochemistry 40 2001 7433 7445
92. D.W. Klumpp, C. Humphrey, H. Huasheng, and F. Tao Toxic contaminants and their biological effects in coastal waters of Xiamen, China. II. Biomarkers and embryp malformation rates as indicators of pollution stress in fish Mar. Pollut. Bull. 44 2002 761 769
93. J.R. Knowles, and W.J. Albery Perfection in enzyme catalysis: the energetics of triosephosphate isomerase Acc. Chem. Res. 10 1977 105 111
94. M.D. Krasowski, D.S. McGehee, and J. Moss Natural inhibitors of cholinesterases: implications for adverse drug reactions Can. J. Anaesth. 44 1997 525 534
95. A. Krause, A.B. Lane, and T. Jenkins A new high activity plasma cholinesterase variant J. Med. Genet. 25 1988 677 681
96. M. Krause, J.D. Leslie, M. Stewart, E.M. Lafuente, F. Valderrama, R. Jaganathan, G.A. Strasser, D.A. Rubinson, H. Liu, M. Way, M.B. Yaffe, V.A. Boussiotis, and F.B. Gertler Lamellipodin, an Ena/VASP ligand, is implemented in the regulation of lamellipodial dynamics Dev. Cell 7 2004 571 583
97. G. Kristoff, N.V. Guerrero, D.M. De D'Angelo, and A.C. Cochon Inhibition of cholinesterase activity by azinphos-methyl in two freshwater invertebrates, Biomphalaria glabrata and Lumbriculus variegatus Toxicology 222 2006 185 194
98. T. Küçükkilinç, R. Cochran, J. Kalisiak, E. Garcia, A. Valle, G. Amitai, Z. Radić, and P. Taylor Investigating the structural influence of surface mutations on acetylcholinesterase inhibition by organophosphate compounds and oxime reactivation Chem. Biol. Interact. 187 2010 238 240
99. R. Lane, H.H. Feldman, J. Meyer, Y. He, S.H. Ferris, A. Nordberg, T. Darreh-Shori, H. Soininen, T. Pirttilä, M.R. Farlow, N. Sfikas, C. Ballard, and N.H. Greig Synergistic effect of apolipoprotein E epsilon 4 and butyrylcholinesterase K-variant on progression from mild cognitive impairment to Alzheimer's disease Pharmacogenet. Genomics 18 2008 289 298
100. P.G. Layer, and O. Sporns Spatiotemporal relationship of embryonic cholinesterases with cell proliferation in chicken brain and eye Proc. Natl. Acad. Sci. USA 84 1987 284 288
101. P.G. Layer, T. Weikert, and R. Alber Cholinesterases regulate neurite outgrowth of chick nerve cells in vitro by means of a non-enzymatic mechanism Cell Tissue Res. 273 1993 219 226
102. P.G. Layer, and E. Willbold Novel functions of cholinesterases in development, physiology and disease Prog. Histochem. Cytochem. 29 1995 1 94
103. D.J. Lehman, C. Johnston, and A.D. Smith Synergy between the genes for butyrylcholinesterase K variant and apolipoprotein E4 in late-onset confirmed Alzheimer's disease Hum. Mol. Genet. 6 1997 1933 1936
104. W.S. Leibel Characterization of a pseudocholinesterase purified from surgeonfish tissues confirms the atypical nature of this enzyme J. Exp. Zool. 247 1988 198 208
105. E. Lev-Lehman, T. Evron, R.S. Broide, E. Meshorer, E. Ariel, S. Seidman, and H. Soreq Synaptogenesis and myopathy under acetylcholinesterase overexpression J. Mol. Neurosci. 14 2000 93 105
106. B. Li, E.G. Duysen, T.L. Saunders, and O. Lockridge Production of the butyrylcholinesterase knockout mouse J. Mol. Neurosci. 30 2006 193 195
107. B. Li, E.G. Duysen, and O. Lockridge The butyrylcholinesterase knockout mouse is obese on a high-fat diet Chem. Biol. Interact. 175 2008 88 91
108. B. Li, J.A. Stribley, A. Ticu, W. Xie, L.M. Schopfer, P. Hammond, S. Brimijoin, S.H. Hinrichs, and O. Lockridge Abundant tissue butyrylcholinesterase and its possible function in acetylcholinesterase knockout mice J. Neurochem. 75 2000 1320 1331
109. H. Li, L.M. Schopfer, P. Masson, and O. Lockridge Lamellipodin proline-rich peptides associated with native plasma butyrylcholinesterase Biochem. J. 411 2008 425 432
110. W.-H. Li Molecular Evolution 1997 Sunderland, MA MA Sinauer Associates
111. O. Lockridge, and B.N. La Du Comparison of atypical and usual human serum cholinesterase: purification, number of active sites, substrate affinity and turnover number J. Biol. Chem. 253 1978 361 366
112. O. Lockridge, and P. Masson Pesticides and susceptible populations: people with butyrylcholinesterase genetic variants may be at risk Neurotoxicology 21 2000 113 126
113. O. Lockridge, E.G. Duysen, T. Voelker, C.M. Thompson, and L.M. Schopfer Life without acetylcholinesterase: the implications of cholinesterase inhibitor toxicity in acetylcholinesterase knockout mice Environ. Toxicol. Pharmacol. 19 2005 463 469
114. Y. Loewenstein-Lichtenstein, M. Schwarz, D. Glick, B. Norgaard-Pedersen, H. Zakut, and H. Soreq Genetic predisposition to adverse consequences of anti-cholinesterases in "atypical" butyrylcholinesterase carriers Nat. Med. 1 1995 1082 1085
115. S.J. Lundin Properties of a cholinesterase from body muscles of plaice (Pleuronectes platessa) Acta Chem. Scand. 22 1968 2183 2190
116. M. Lynch The evolutionary fate and consequences of duplicate genes Science 290 2000 1151 1155
117. H. Mabrouk, H. Mechri, A. Mechri, H. Rahali, W. Douki, L. Gaha, and N.M. Fadhel Butyrylcholinesterase activity in schizophrenic patients Ann. Biol. Clin. (Paris) 69 2011 649 652
118. A. Mack, and A. Robitzki The key role of butyrylcholinesterase during neurogenesis and neural disorders: an antisense-5′-butyrylcholinesterase- DNA study Prog. Neurobiol. 60 2000 607 628
119. M. Maekawa, K. Sudo, D.C. Dey, J. Ishikawa, M. Izumi, K. Kotani, and T. Kanno Genetic mutations of butyrylcholine esterase identified from phenotypic abnormalities in Japan Clin. Chem. 43 1997 924 929
120. G.J. Maletta, and P.S. Timiras Acetyl- and butyrylcholinesterase activity of selected brain areas in developing rats after neonatal X-irradiation J. Neurochem. 13 1966 75 84
121. I. Manoharan, A. Kuznetsova, J.D. Fisk, R. Boopathy, O. Lockridge, and S. Darvesh Comparison of cognitive functions between people with silent and wild-type butyrylcholinesterase J. Neural Transm. 114 2007 939 945
122. P. Martinez-Moreno, S. Nieto-Cerón, J. Torres-Lanzas, F. Ruiz-Espejo, I. Tovar-Zapata, P. Martinez-Hernandez, J.N. Rodriguez-Lopez, C.J. Vidal, and J. Cabezas-Herrera Cholinesterase activity of human lung tumours varies according to their histological classification Carcinogenesis 27 2006 429 436
123. P. Masson A naturally occurring molecular form of human plasma cholinesterase is an albumin conjugate Biochim. Biophys. Acta 998 1989 258 266
124. P. Masson Molecular heterogeneity of human plasma cholinesterase J. Massoulié, F. Bacou, E. Barnard, A. Chatonnet, B.P. Doctor, D.M. Quinn, Cholinesterases. Structure, Function, Mechanisms, Genetics and Cell Biology 1991 American Chemical Society Washington D.C. 42 45
125. P. Masson, M.T. Froment, C.F. Bartels, and O. Lockridge Importance of aspartate70 in organophosphate inhibition, oxime re-activation and aging of human butyrylcholinesterase Biochem. J. 325 1997 53 61
126. P. Masson, and O. Lockridge Butyrylcholinesterase for protection from organophosphate poisons: catalytic complexities and hysteretic behavior Arch. Biochem. Biophys. 494 2010 107 120
127. J. Massouliè, L. Pezzementi, S. Bon, E. Krejci, and F.M. Valette Molecular and cellular biology of cholinesterases Prog. Neurobiol. 41 1993 31 91
128. J. Massouliè The origin of the molecular diversity and functional anchoring of cholinesterases Neurosignals 11 2002 130 143
129. J. Massouliè, S. Bon, N. Perrier, and C. Falasca The C-terminal peptides of acetylcholinesterase: cellular trafficking, oligomerization and functional anchoring Chem. Biol. Interact. 157-158 2005 3 14
130. J.S. McClellan, W.B. Coblentz, M. Sapp, G. Rulewicz, D.I. Gaines, A. Hawkins, C. Ozment, A. Bearden, S. Merritt, J. Cunningham, E. Palmer, A. Contractor, and L. Pezzementi cDNA cloning, in vitro expression, and biochemical characterization of cholinesterase 1 and cholinesterase 2 from amphioxus - comparison with cholinesterase 1 and cholinesterase 2 produced in vivo Eur. J. Biochem. 258 1998 419 429
131. D.C. McGehee, M.D. Krasowski, D.L. Fung, B. Wilson, G.A. Gronert, and J. Moss Cholinesterase inhibition by potato glycoalkaloids slows mivacurium metabolism Anesthesiology 93 2000 510 519
132. M.C. McGuire, C.P. Nogueira, C.F. Bartels, H. Lightstone, A. Hajra, A.E. Van der Spek, O. Lockridge, and B.N. La Du Identification of the structural mutation responsible for the dibucaine-resistant (atypical) variant form of serum cholinesterase Proc. Natl. Acad. Sci. USA 86 1989 953 957
133. E. Meshorer, and H. Soreq Virtues and woes of acetylcholinesterase alternative splicing in stress-related neuropathologies Trends Neurosci. 29 2006 216 224
134. M.M. Mesulam, C. Geula, S. Brimijoin, and J.F. Smiley Butyrylcholinesterase immunochemistry in human cerebral cortex Soc. Neurosci. Abstr. 21 1995 1976
135. M.M. Mesulam Neuroanatomy of cholinesterases in the normal human brain and in Alzheimer's disease E. Giacobini, Cholinesterases and Cholinesterase Inhibitors 2000 Martin Dinitz London 121 138
136. M.M. Mesulam, A. Guillozet, P. Shaw, A. Levey, E.G. Duysen, and O. Lockridge Acetylcholinesterase knockouts establish central cholinergic pathways and can use butyrylcholinesterase to hydrolyse acetylcholine Neuroscience 110 2002 627 639
137. L.R. Mikami, S. Wieseler, R.L. Souza, L.M. Schopfer, F. Nachon, O. Lockridge, and E.A. Chautard-Freire-Maia Five new naturally occurring mutations of the BCHE gene and frequencies of 12 butyrylcholinesterase alleles in a Brazilian population Pharmacogenet. Genomics 18 2008 213 218
138. J. Minic, A. Chatonnet, E. Krejci, and J. Molgó Butyrylcholinesterase and acetylcholinesterase activity and quantal transmitter release at normal and acetylcholinesterase knockout neuromuscular junctions Br. J. Pharmacol. 138 2003 177 187
139. E. Muňoz-Delgado, M.F. Montenegro, J.C. Morote-Garcia, F.J. Campoy, J. Cabezas-Herrera, G. Kovacs, and C.J. Vidal The expression of cholinesterases in human renal tumours varies according to their histological types Chem. Biol. Interact. 175 2005 340 342
140. E. Muňoz-Delgado, M.F. Montenegro, F.J. Campoy, M.T. Moral-Naranjo, J. Cabezas-Herrera, G. Kovacs, and C.J. Vidal Expression of cholinesterases in human kidney and its variation in renal cell carcinoma types FEBS J. 277 2010 4519 4529
141. L.F. Neville, A. Gnatt, Y. Loewenstein, and H. Soreq Aspartate-70 to glycine substitution confers resistance to naturally occurring and synthetic anionic-site ligands on in-ovo produced human butyrylcholinesterase J. Neurosci. Res. 27 1990 452 460
142. L.F. Neville, A. Gnatt, Y. Loewenstein, S. Seidman, G. Ehrlich, and H. Soreq Intramolecular relationships in cholinesterase revealed by oocyte expression of site-directed and natural variants of human BCHE EMBO J. 11 1992 1641 1649
143. Y. Nicolet, O. Lockridge, P. Masson, J.C. Fonticella-Camps, and F. Nachon Crystal structure of human butyrylcholinesterase and of its complexes with substrate and products J. Biol. Chem. 273 2003 41141 41147
144. K.K. O'Brien, B.K. Saxby, C.G. Ballard, J. Grace, F. Harrington, G.A. Ford, J.T. O'Brien, A.G. Swan, A.F. Fairbairn, K. Westes, T. del Sol, J.A. Edwardson, C.M. Morris, and I.G. McKeith Regulation of attention and response to thrapy in dementia by butyrylcholinesterase Pharmacogenetics 13 2003 231 239
145. S. Ohno Evolution by Gene Duplication 1970 Springer-Verlag New York
146. M.S. Omar, A.M. Raoof, and O.M. al-Amari Histochemical distribution of esterases in adult Onchocerca fasciata (Filarioidea: Onchocercidae) Trop. Med. Parasitol. 44 1993 295 298
147. A. Ordentlich, D. Barak, C. Kronman, Y. Flashner, M. Leitner, Y. Segall, N. Ariel, S. Cohen, B. Velan, and A. Shafferman Dissection of the human acetylcholinesterase active center determinants of substrate specificity: identification of residues consituting the anionic site, the hydrophobic site and the acyl pocket J. Biol. Chem. 268 1993 17083 17095
148. I.E. Orhan Current concepts on selected plant secondary metabolites with promising effects against enzymes linked to Alzheimer's disease Curr. Med. Chem. 19 2012 2252 2261
149. H.A. Orr A test of Fisher's theory of dominance Proc. Natl. Acad. Sci. USA 88 1991 11413 11415
150. L.E. Paraoanu, and P.G. Layer Acetylcholinesterase in cell adhesion, neurite outgrowth and network formation FEBS J. 275 2008 618 624
151. G. Perea, and A. Araque Properties of synaptically evoked astrocyte calcium signal reveal synaptic information processing by astrocytes J. Neurosci. 25 2005 2192 2203
152. G. Perea, M. Navarrete, and A. Araque Tripartite synapses: astrocytes process and control synaptic information Trends Neurosci. 32 2009 421 431
153. A. Pereira Jr., and F.A. Furlon Astrocytes and human cognition: modeling
154. E. Perry, I. McKeith, and C. Ballard Butyrylcholinesterase and progression of cognitive deficits in dementia with Lewy bodies Neurology 60 2003 1552 1553
155. E.K. Perry, R.H. Perry, G. Blessed, and B.E. Tomlinson Changes in brain cholinesterases in senile dementia of Alzheimer type Neuropathol. Appl. Neurobiol. 4 1978 273 277
156. L. Pezzementi, K. Johnson, I. Tsigelny, J. Cotney, E. Manning, A. Barker, and S. Merritt Amino acids defining the acyl pocket of an invertebrate cholinesterase Comp. Biochem. Physiol. B Biochem. Mol. Biol. 136 2003 813 832
157. L. Pezzementi, and A. Chatonnet Evolution of cholinesterases in the animal kingdom Chem. Biol. Interact. 187 2010 27 33
158. L. Pezzementi, F. Nachon, and A. Chatonnet Evolution of acetylcholinesterase and butyrylcholinesterase in the vertebrates: an atypical butyrylcholinesterase from the medaka Oryzias latipes PLoS One 6 2011 e17396
159. L. Pezzementi, E.J. Reinheimer, and M.L. Pezzementi Acetylcholinesterase from the skeletal muscle of the lamprey Petromyzon marinus exists in globular and asymmetric forms J. Neurochem. 48 1987 1753 1760
160. E. Podoly, D.E. Shalev, S. Shenhar-Tsarfaty, E.R. Bennett, E. Ben Assayag, H. Wilgus, O. Livnah, and H. Soreq The butyrylcholinesterase K variant confers structurally derived risks for Alzheimer pathology J. Biol. Chem. 284 2009 17170 17179
161. S.L. Primo-Parmo, C.F. Bartels, B. Wiersema, A.F. Van der Spek, J.W. Innis, and B.N. La Du Characterization of 12 silent alleles of the human butyrylcholinesterase (BCHE) gene Am. J. Hum. Genet. 58 1996 52 64
162. C.A. Prody, D. Zevin-Sonkin, A. Gnatt, O. Goldberg, and H. Soreq Isolation and characterization of full-length cDNA clones coding for cholinesterase from fetal human tissue Proc. Natl. Acad. Sci. USA 84 1987 3555 3559
163. N.H. Putnam, T. Butts, D.E.K. Ferrier, and R.F. Furlong The amphioxus genome and the evolution of the chordate karyotype Nature 453 2008 1064 1072
164. Z. Radic, R. Duran, D.C. Vellom, Y. Li, C. Cervenansky, and P. Taylor Site of fasciculin interaction with acetylcholinesterase J. Biol. Chem. 269 1994 11233 11239
165. Z. Radic, N.A. Pickering, D.C. Vellom, S. Camp, and P. Taylor Three distinct domains in the cholinesterase molecule confer selectivity for acetyl- and butyrylcholinesterase inhibitors Biochemistry 32 1993 12074 12084
166. L. Raveh, E. Grauer, J. Grunwald, E. Cohen, and Y. Ashani The stoichiometry of protection against soman and VX toxicity in monkeys pretreated with human butyrylcholinesterase Toxicol. Appl. Pharmacol. 145 1997 43 53
167. M. Raymond, C. Chevillon, T. Guillemaud, T. Lenormand, and N. Pasteur An overview of the evolution of overproduced esterases in the mosquito Culex pipiens. Philos Trans. R. Soc. Lond. B Biol. Sci. 353 1998 1707 1711
168. M.C. Reed, A. Lieb, and H.F. Nijhout The biological significance of substrate inhibition: a mechanism with diverse functions Bioessays 32 2010 422 429
169. L. Renault, V. Nègre, T. Hotelier, X. Cousin, P. Marchot, and A. Chatonnet New friendly tools for users of ESTHER, the database of the alpha/beta hydrolase fold superfamily of proteins Chem. Biol. Interact. 157-158 2005 339 343
170. H. Repke, and K. Madersprach Muscarinic acetylcholine receptos on cultured glial cells Brain Res. 232 1982 206 211
171. A. Robitzki, F. Döll, C. Richter-Landsberg, and P.G. Layer Regulation of the rat oligodendroglia cell line OLN-93 by antisense transfection of butyrylcholinesterase Glia 31 2000 195 203
172. T.L. Rosenberry Catalysis by acetylcholinesterase: evidence that the rate-limiting step for acylation with certain substrates precedes general acid-base catalysis Proc. Natl. Acad. Sci. USA 72 1975 3834 3838
173. T.L. Rosenberry Strategies to resolve the catalytic mechanism of acetylcholinesterase J. Mol. Neurosci. 40 2010 32 39
174. R.C. Ros-Moreno, C. De Armas-Serra, C. Giminez-Pardo, and F. Rodriguez-Caabeiro Comparison of cholinesterase activities in the excretion-secretion products of Trichinella pesudospiralis and Trichinella spiralis muscle larvae Parasite 9 2002 153 159
175. J. Sáez-Valero, P.L. Tornel, E. Muňoz-Delgado, and C.J. Vidal Amphiphilic and hydrophilic forms of acetyl- and butyrylcholinesterase in human brain J. Neurosci. Res. 35 1993 678 689
176. M. Sanders, B. Mathews, D. Sutherland, W. Soong, M. Giles, and L. Pezzementi Biochemical and molecular characterization of acetylcholinesterase from the hagfish Myxine glutinosa Comp. Biochem. Physiol. B Biochem. Mol. Biol. 115 1996 97 109
177. A. Saxena, L. Raveh, Y. Ashani, and B.P. Doctor Structure of glycan moieties responsible for the extended circulatory life time of fetal bovine serum acetylcholinesterase and equine serum butyrylcholinesterase Biochemistry 36 1997 7481 7489
178. A. Saxena, A.M. Redman, X. Jiang, O. Lockridge, and B.P. Doctor Differences in active site gorge dimensions of cholinesterases revealed by binding of inhibitors to human butyrylcholinesterase Biochemistry 36 1997 14642 14651
179. A. Saxena, W. Sun, C. Luo, T.M. Myers, I. Koplovitz, D.E. Lenz, and B.P. Doctor Bioscavenger for protection from toxicity of organophosphate compounds J. Mol. Neurosci. 30 2006 145 148
180. A. Shafferman, B. Velan, A. Ordentlich, C. Kronman, H. Grosfeld, M. Leitner, Y. Flashner, S. Cohen, D. Barak, and N. Ariel Substrate inhibition of acetylcholinesterase: residues affecting signal transduction from the surface to the catalytic center EMBO J. 11 1992 3561 3568
181. S. Shenhar-Tsarfaty, T. Bruck, E.R. Bennett, T. Bravman, E.B. Aassayag, N. Waiskopf, O. Rogowski, N. Bornstein, S. Berliner, and H. Soreq Butyrylcholinesterase interactions with amylin may protect pancreatic cells in metabolic syndrome J. Cell. Mol. Med. 15 2011 1747 1756
182. I. Silman, and J.L. Sussman Acetylcholinesterase: how is structure related to function? Chem. Biol. Interact. 175 2008 3 10
183. A. Silver The Biology of Cholinesterases 1974 North-Holland/American Elsevier Amsterdam-New York
184. S. Singh, V. Kumar, S. Thakut, B.D. Banerjee, S. Chandna, R.S. Rautela, S.S. Grover, D.S. Rawat, S.T. Pasha, S.K. Jain, R.L. Ichipujani, and A. Rai DNA damage and cholinesterase activity in occupational workers exposed to pesticides Environ. Toxicol. Pharmacol. 31 2011 278 285
185. T. Sişman Dichlorvos-induced developmental toxicity in zebrafish Toxicol. Ind. Health 26 2010 567 573
186. A.B. Smit, N.I. Syed, D. Schaap, J. Van Minnen, J. Klumperman, K.S. Kits, H. Lodder, R.C. Van der Schors, R. Van Elk, B. Sorgedrager, K. Brejc, T.H. Sixma, and W.P.H. Geraerts A glia-derived acetylcholine-binding protein that modulates synaptic neurotransmission Nature 411 2001 261 268
187. M.A. Sogorb, and E. Vilanova Serum albumins and detoxification of anti-cholinesterase agents Chem. Biol. Interact. 187 2010 325 329
188. H. Soreq, R. Ben-Aziz, C.A. Prody, S. Seidman, A. Gnatt, L. Neville, J. Lieman-Hurwitz, E. Lev-Lehman, D. Ginzberg, Y. Lapidot-Lifson, and H. Zakut Molecular cloning and construction of the coding region for human acetylcholinesterase reveals a G+C-rich attenuating structure Proc. Natl. Acad. Sci. USA 87 1990 9688 9692
189. N. Sorobyan, S. Jagannathan, I. Orlovskaya, I. Schraufstatter, M. Skok, J. Loring, and S. Khaldoyanidu The cholinergic system is involved in regulation of the development of the hematopoietic system Life Sci. 80 2007 2352 2360
190. R.L. Souza, L. Furtado, A.C. Diniz, A.C. Silva, J. Kaiss, M.L. Petzl-Erler, and E.A. Chautard-Freire-Maia Studies on a heterologous complex formed by human butyrylcholinesterase Biochem. Genet. 41 2003 141 150
191. R.L. Souza, C. Fadel-Picheth, K.V. Allebrandt, L. Furtado, and E.A. Chautard-Freire-Maia Possible influence of BCHE locus of butyrylcholinesterase on stature and body mass index Am. J. Phys. Anthropol. 126 2005 329 334
192. R.L. Souza, L.R. Mikami, R.O. Maegawa, and E.A. Chautard-Freire-Maia Four new mutations in the BCHE gene of human butyrylcholinesterase in a Brazilian blood donor sample Mol. Genet. Metab. 84 2005 349 353
193. L.E. Sperling, G. Steinert, J. Boutter, D. Landgraf, J. Heschler, D. Pollet, and P.G. Layer Characterisation of cholinesterase expression during murine embryonic stem cell differentiation Chem. Biol. Interact. 175 2008 156 160
194. L.E. Sperling, J. Klaczinski, C. Schtz, L. Rudolph, and P.G. Layer Mouse acetylcholinesterase enhances neurite outgrowth of rat r28 cells through interaction with laminin-1 PLoS One 7 2012 e36683
195. S. Stieger, R. Gentinetta, and U. Brodbeck Cholinesterases from flounder muscle. Purification and characterization of glycosyl-phosphatidylinositol- anchored and collagen-tailed forms differing in substrate specificity Eur. J. Biochem. 181 1989 633 642
196. M. Suhail, and S.I. Rizvi Erythrocyte membrane acetylcholinesterase in type I (insulin-dependent) diabetes mellitus Biochem. J. 259 1989 897 899
197. J.L. Sussman, M. Harel, F. Frolow, C. Oefner, A. Goldman, L. Toker, and I. Silman Atomic structure of acetylcholinesterase from Torpedo californica, a prototypic acetylcholine-binding protein Science 253 1991 872 879
198. D. Sutherland, J.S. McClellan, D. Milner, W. Soong, N. Axon, M. Sanders, A. Hester, Y.H. Kao, T. Poczatek, S. Routt, and L. Pezzementi Two cholinesterase activities and genes are present in amphioxus J. Exp. Zool. 277 1997 213 229
199. J.-P. Toutant, J. Massouliè, and S. Bon Polymorphism of pseudocholinesterase in Torpedo marmorata tissues: comparative study of the catalytic and molecular properties of this enzyme with acetylcholinesterase J. Neurochem. 44 1985 580 592
200. A. Vaisi-Raygani, Z. Rahimi, H. Tavilani, and T. Pourmotabbed Butyrylcholinesterase K variant and the APOE-epsilon 4 allele work in synergy to increase the risk of coronary artery disease especially in diabetic patients J. Neural. Transm. 117 2010 377 383
201. A. Valle, D.T. O'Connor, P. Taylor, G. Zhu, G.W. Montgomery, P.E. Slagboom, N.G. Martin, and J.B. Whitfield Butyrylcholinesterase: association with the metabolic syndrome and identification of two gene loci affecting activity Clin. Chem. 52 2006 1014 1020
202. D.C. Vellom, Z. Radic, Y. Li, N.A. Pickering, S. Camp, and P. Taylor Amino acid residues controlling acetylcholinesterase and butyrylcholinesterase specificity Biochemistry 32 1993 12 17
203. A. Verkhratsky, R.K. Orkand, and H. Kettenman Glial calcium: homeostasis and signaling function Physiol. Rev. 78 1998 99 141
204. C.J. Vidal Expression of cholinesterases in brain and non-brain tumours Chem. Biol. Interact. 157-158 2005 227 232
205. A. Vioque-Fernandez, E.A. De Almeida, and J. Lopez-Barea Esterases as pesticide biomarkers in crayfish (Procambarus clarkii; Crustacea): tissue distribution, sensitivity to model compounds and recovery from inactivation Comp. Biochem. Physiol. C Toxicol. Pharmacol. 145 2007 404 412
206. E. Weitnauer, C. Ebert, F. Hucho, A. Robitzki, C. Weise, and P.G. Layer Butyrylcholinesterase is complexed with transferrin in chicken serum J. Protein Chem. 18 1999 205 214
207. I. Wessler, and C.J. Kirkpatrick Acetylcholine beyond neurons: the non-neuronal cholinergic system in humans Br. J. Pharmacol. 154 2008 1558 1571
208. I. Wessler, T. Reinheiner, H. Klapproth, F.J. Schneider, K. Racké, and R. Hammer Mammalian glial cells in culture synthesise acetylcholine Naunyn Schmiedebergs Arch. Pharmacol. 356 1997 694 697
209. M. Whittaker, and J.J. Britten Recognition of two new phenotypes segregating the E1k allele for plasma cholinesterase Hum. Hered. 38 1988 233 239
210. V.P. Whittaker How the cholinesterases got their modern names Chem. Biol. Interact. 187 2010 23 26
211. J.M. Wierenga, and R.M. Hollingworth Inhibition of insect acetylcholinesterase by the potato glycoalkaloid alpha-chaconine Nat. Toxins 1 1992 96 99
212. I.B. Wilson, and J. Alexander Acetylcholinesterase: reversible inhibitors, substrate inhibition J. Biol. Chem. 237 1962 1323 1326
213. W. Xie, C.V. Altamirano, C.F. Bartels, R.J. Speirs, J.R. Cashman, and O. Lockridge An improved cocaine hydrolase: the A328Y mutant of human butyrylcholinesterase is 4-fold more efficient Mol. Pharmacol. 55 1999 83 91
214. W. Xie, J.A. Stribley, A. Chatonnet, P.J. Wilder, A. Rizzino, R.D. McComb, P. Taylor, S.H. Hinrichs, and O. Lockridge Postnatal developmental delay and supersensitivity to organophosphates in gene-targeted mice lacking acetylcholinesterase J. Pharmacol. Exp. Ther. 293 2000 896 902
215. Y. Xu, J.P. Colletier, M. Weik, H. Jiang, J. Moult, I. Silman, and J.L. Sussman Flexibility of aromatic residues in the active-site gorge of acetylcholinesterase: x-ray versus molecular dynamics Biophys. J. 95 2008 2500 2511
216. J. Yanai, A. Pinkas, F.J. Seidler, I.T. Ryde, E.A. Van der Zee, and T.A. Slotkin Neurobehavioral teratogenicity of sarin in an avian model Neurotoxicol. Teratol. 31 2009 406 412
217. D.Y. Yoo, Y.J. Woo, W. Kim, S.M. Nam, B.H. Lee, G.H. Yeun, Y.S. Yoon, M.N. Won, J.H. Park, and I.K. Hwang Effects of a new synthetic butyrylcholinesterase inhibitor, MBU-39, on cell proliferation and neuroblast differentiation in the hippocampal dentate gyrus in a scopolamine-induced amnesia animal model Neurochem. Int. 59 2011 722 728
218. A. Yoshida, and A.G. Motulsky A pseudocholinesterase variant (E Cynthiana) associated with elevated plasma enzyme activity Am. J. Hum. Genet. 21 1969 486 489
219. N. Zhang, and J.E. Casida Novel irreversible butyrylcholinesterase inhibitors: 2-chloro-1-(substituted-phenyl) ethylphosphonic acids Bioorg. Med. Chem. 10 2002 1281 1290
220. D.M. Ziegler The 1990 Bernard B. Brodie Lecture: unique properties of the enzymes of detoxification Drug Metab. Dispos. 19 1991 847 852