The origin of the molecular diversity and functional anchoring of cholinesterases

NeuroSignals

Volumn 11, Issue 3, 2002, Pages 130-143

  Massoulié, Jean ^a  

^a ECOLE NORMALE SUPÉRIEURE   (France)

Author keywords

Alternative splicing; Basal lamina; Cholinesterase; GPI; Membrane anchoring

Indexed keywords

ACETYLCHOLINESTERASE; AMYLOID BETA PROTEIN; BACTERIAL PROTEIN; CHOLINESTERASE; COLLAGEN; COLLAGEN DERIVATIVE; GLYCOSYLPHOSPHATIDYLINOSITOL; PROTEIN SUBUNIT; B230212M13RIK PROTEIN, MOUSE; CHOLINESTERASE INHIBITOR; COLQ PROTEIN, HUMAN; MEMBRANE PROTEIN; MUSCLE PROTEIN; NERVE PROTEIN; PRIMA1 PROTEIN, HUMAN;

ALPHA HELIX; ALZHEIMER DISEASE; AMYLOIDOSIS; BASEMENT MEMBRANE; BLOOD CELL; BRAIN; CAENORHABDITIS ELEGANS; CARBOXY TERMINAL SEQUENCE; CATALYSIS; DROSOPHILA; EMBRYONAL TISSUE; ENZYME SPECIFICITY; EXERCISE; EXTRACELLULAR MATRIX; GENE MUTATION; GENETIC VARIABILITY; HEMATOPOIETIC CELL; HUMAN; HYDROLYSIS; MAMMAL; MUSCLE; NEUROFIBRILLARY TANGLE; NEUROMUSCULAR SYNAPSE; NONHUMAN; OOCYTE; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; REVIEW; STRESS; XENOPUS; ALTERNATIVE RNA SPLICING; AMINO ACID SEQUENCE; ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; CLASSIFICATION; GENETICS; MACROMOLECULE; METABOLISM; MOLECULAR GENETICS; MOUSE; MOUSE MUTANT; PHYSIOLOGY; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN PROCESSING; PROTEIN TERTIARY STRUCTURE; TORPEDO; VERTEBRATE;

ACETYLCHOLINESTERASE; ALTERNATIVE SPLICING; AMINO ACID SEQUENCE; ANIMALS; BUTYRYLCHOLINESTERASE; CHOLINESTERASE INHIBITORS; CHOLINESTERASES; COLLAGEN; GLYCOSYLPHOSPHATIDYLINOSITOLS; HUMANS; MACROMOLECULAR SUBSTANCES; MEMBRANE PROTEINS; MICE; MICE, KNOCKOUT; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUSCLE PROTEINS; NERVE TISSUE PROTEINS; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STRUCTURE, TERTIARY; PROTEIN SUBUNITS; SUBSTRATE SPECIFICITY; TORPEDO; VERTEBRATES;

EID: 0036560908     PISSN: 1424862X     EISSN: None     Source Type: Journal    
DOI: 10.1159/000065054     Document Type: Review

References (99)

1. Radic Z, Quinn DM, Vellom DC, Camp S, Taylor P: Amino acid residues in acetylcholinesterase which influence fasciculin inhibition; in Quinn DM, Balasubramanian AS, Doctor BP, Taylor P (eds): Enzymes of the Cholinesterase Family. New York, Plenum, 1995, pp 183-188.
2. Massoulié J, Bon S: The molecular forms of cholinesterase and acetylcholinesterase in vertebrates. Annu Rev Neurosci 1982;5:57-106.
3. Hall LMC, Spierer P: The Ace locus of Drosophila melanogaster: Structural gene for acetylcholinesterase with an unusual 5′ leader. EMBO J 1986;5:2949-2954.
4. Combes D, Fedon Y, Grauso M, Toutant J-P, Arpagaus M: Four genes encode acetylcholinesterases in the nematodes Caenorhabditis elegans and Caenorhabditis briggsae. cDNA sequences, mutations and in vivo expression. J Mol Biol 2000;300:727-742.
5. Massoulié J, Pezzementi L, Bon S, Krejci E, Vallette FM: Molecular and cellular biology of cholinesterases. Prog Neurobiol 1993;41:31-91.
6. Arpagaus M, Kott M, Vatsis KP, Bartels CF, La Du BN, Lockridge O: Structure of the gene for human butyrylcholinesterase. Evidence for a single copy. Biochemistry 1990;29:124-131.
7. Giacobini E (ed): Cholinesterases and Cholinesterase Inhibitors. London, Martin Dunitz, 2000.
8. Whittaker M: Cholinesterase. Monogr Hum Genet. Basel, Karger, 1986, vol 11, p 132.
9. Bartels CF, James K, La Du BN: DNA mutations associated with the human butyrylcholinesterase J-variant. Am J Hum Genet 1992;50:1104-1114.
10. Bartels CF, Jensen FS, Lockridge O, van der Spek AF, Rubinstein HM, Lubrano T, La Du BN: DNA mutation associated with the human butyrylcholinesterase K-variant and its linkage to the atypical variant mutation and other polymorphic sites. Am J Hum Genet 1992;50: 1086-1103.
11. Lockridge O, Masson P: Pesticides and susceptible populations: People with butyrylcholinesterase genetic variants may be at risk. Neurotoxicology 2000;21:113-126.
12. Neville LF, Gnatt A, Loewenstein Y, Soreq H: Aspartate-70 to glycine substitution confers resistance to naturally occurring and synthetic anionic-site ligands on in-ovo produced human butyrylcholinesterase. J Neurosci Res 1990;27:452-460.
13. Sun H, El Yazal J, Lockridge O, Schopfer LM, Brimijoin S, Pang YP: Predicted Michaelis-Menten complexes of cocaine-butyrylcholinesterase. Engineering effective butyrylcholinesterase mutants for cocaine detoxication. J Biol Chem 2001;276:9330-9336.
14. Sussman JL, Harel M, Frolow F, Oefner C, Goldman A, Toker L, Silman I: Atomic structure of acetylcholinesterase from Torpedo californica: A prototypic acetylcholine-binding protein. Science 1991;253:872-879.
15. Bourne Y, Taylor P, Marchot P: Acetylcholinesterase inhibition by fasciculin: Crystal structure of the complex. Cell 1995;83:503-512.
16. Marchot P, Ravelli RB, Raves ML, Bourne Y, Vellom DC, Kanter J, Camp S, Sussman JL, Taylor P: Soluble monomeric acetylcholinesterase from mouse: Expression, purification, and crystallization in complex with fasciculin. Protein Sci 1996;5:672-679.
17. Harel M, Kryger G, Rosenberry TL, Mallender WD, Lewis T, Fletcher RJ, Guss JM, Silman I, Sussman JL: Three-dimensional structures of Drosophila melanogaster acetylcholinesterase and of its complexes with two potent inhibitors. Protein Sci 2000;9:1063-1072.
18. Nachon F, Nicolet Y, Viguié N, Masson P, Fontecilla-Camps JC, Lockridge O: Engineering of a monomeric and low-glycosylated form of human butyrylcholinesterase: Expression, purification, characterization and crystallization. Eur J Biochem 2002;269:630-637.
19. Ollis DL, Cheah E, Cygler M, Dijkstra B, Frolow F, Franken SM, Harel M, Remington SJ, Silman I, Schrag J, Sussman JL, Verschueren KHG, Goldman A: The alpha/beta hydrolase fold. Protein Eng 1992;5:197-211.
20. Cousin X, Hotelier T, Giles K, Toutant JP, Chatonnet A: aCHEdb: The database system for ESTHER, the alpha/beta fold family of proteins and the cholinesterase gene server. Nucleic Acids Res 1998;26:226-228.
21. Harel M, Sussman JL, Krejci E, Bon S, Chanal P, Massoulié J, Silman I: Conversion of acetylcholinesterase to butyrylcholinesterase: Modeling and mutagenesis. Proc Natl Acad Sci USA 1992;89:10827-10831.
22. Kraut D, Goff H, Pai RK, Hosea NA, Silman I, Sussman JL, Taylor P, Voet JG: Inactivation studies of acetylcholinesterase with phenylmethylsulfonyl fluoride. Mol Pharmacol 2000;57: 1243-1248.
23. Radic Z, Pickering NA, Vellom DC, Camp S, Taylor P: Three distinct domains in the cholinesterase molecule confer selectivity for acetyl- and butyrylcholinesterase inhibitors. Biochemistry 1993;32:12074-12084.
24. Vellom DC, Radic Z, Li Y, Pickering NA, Camp S, Taylor P: Amino acid residues controlling acetylcholinesterase and butyrylcholinesterase specificity. Biochemistry 1993;32:12-17.
25. Mallender WD, Szegletes T, Rosenberry TL: Acetylthiocholine binds to asp74 at the peripheral site of human acetylcholinesterase as the first step in the catalytic pathway. Biochemistry 2000;39:7753-7763.
26. Szegletes T, Mallender WD, Thomas PJ, Rosenberry TL: Substrate binding to the peripheral site of acetylcholinesterase initiates enzymatic catalysis. Substrate inhibition arises as a secondary effect. Biochemistry 1999;38:122-133.
27. Pörschke D, Créminon C, Cousin X, Bon C, Sussman J, Silman I: Electrooptical measurements demonstrate a large permanent dipole moment associated with acetylcholinesterase. Biophys J 1996;70:1603-1608.
28. Ripoll DR, Faerman CH, Axelsen PH, Silman I, Sussman JL: An electrostatic mechanism for substrate guidance down the aromatic gorge of acetylcholinesterase. Proc Natl Acad Sci USA 1993;90:5128-5132.
29. Tan RC, Truong TN, McCammon JA, Sussman JL: Acetylcholinesterase: Electrostatic steering increases the rate of ligand binding. Biochemistry 1993;32:401-403.
30. Shafferman A, Ordentlich A, Barak D, Kronman C, Ber R, Bino T, Ariel N, Osman R, Velan B: Electrostatic attraction by surface charge does not contribute to the catalytic efficiency of acetylcholinesterase. EMBO J 1994;13:3448-3455.
31. Morel N, Bon S, Greenblatt HM, Van Belle D, Wodak SJ, Sussman JL, Massoulié J, Silman I: Effect of mutations within the peripheral anionic site on the stability of acetylcholinesterase. Mol Pharmacol 1999;55:982-992.
32. Gilson MK, Straatsma TP, McCammon JA, Ripoll DR, Faerman CH, Axelsen PH, Silman I, Sussman JL: Open 'back door' in a molecular dynamics simulation of acetylcholinesterase. Science 1994;263:1276-1278.
33. Kronman C, Ordentlich A, Barak D, Velan B, Shafferman A: The 'back door' hypothesis for product clearance in acetylcholinesterase challenged by site-directed mutagenesis. J Biol Chem 1994;269:27819-27822.
34. Simon S, Le Goff A, Frobert Y, Grassi J, Massoulié J: The binding sites of inhibitory monoclonal antibodies on acetylcholinesterase. Identification of a novel regulatory site at the putative 'back door'. J Biol Chem 1999:274:27740-27746.
35. Massoulié J, Anselmet A, Bon S, Krejci E, Legay C, Morel N, Simon S: Acetylcholinesterase: C-terminal domains, molecular forms and functional localization. J Physiol (Paris) 1998;92:183-190.
36. Legay C, Bon S, Massoulié J: Expression of a cDNA encoding the glycolipid-anchored form of rat acetylcholinesterase. FEBS Lett 1993;315:163-166.
37. Li Y, Camp S, Rachinsky TL, Getman D, Taylor P: Gene structure of mammalian acetylcholinesterase. Alternative exons dictate tissue-specific expression. J Biol Chem 1991;266:23083-23090.
38. Li Y, Camp S, Taylor P: Tissue-specific expression and alternative mRNA processing of the mammalian acetylcholinesterase gene. J Biol Chem 1993;268:5790-5797.
39. Kaufer D, Friedman A, Seidman S, Soreq H: Acute stress facilitates long-lasting changes in cholinergic gene expression. Nature 1998;393:373-377.
40. Meshorer E, Erb C, Gazit R, Pavlovsky L, Kaufer D, Friedman A, Glick D, Ben-Arie N, Soreq H: Alternative splicing and neuritic mRNA translocation under long-term neuronal hypersensitivity. Science 2002;295:508-512.
41. Cousin X, Bon S, Duval N, Massoulié J, Bon C: Cloning and expression of acetylcholinesterase from Bungarus fasciatus venom. A new type of COOH-terminal domain; involvement of a positively charged residue in the peripheral site. J Biol Chem 1996;271:15099-15108.
42. Cousin X, Bon S, Massoulié J, Bon C: Identification of a novel type of alternatively spliced exon from the acetylcholinesterase gene of Bungarus fasciatus. Molecular forms of acetyl-cholinesterase in the snake liver and muscle. J Biol Chem 1998;273:9812-9820.
43. Frobert Y, Créminon C, Cousin X, Rémy MH, Chatel JM, Bon S, Bon C, Grassi J: Acetylcholinesterases from Elapidae snake venoms: Biochemical, immunological and enzymatic characterization. Biochim Biophys Acta 1997;1339:253-267.
44. Cousin X, Créminon C, Grassi J, Méflah K, Cornu G, Saliou B, Bon S, Massoulié J, Bon C: Acetylcholinesterase from Bungarus venom: A monomeric species. FEBS Lett 1996;387:196-200.
45. Ferguson MA, Duszenko M, Lamont GS, Overath P, Cross GA: Biosynthesis of Trypanosoma brucei variant surface glycoproteins. N-glycosylation and addition of a phosphatidylinositol membrane anchor. J Biol Chem 1986;261:356-362.
46. Coussen F, Ayon A, Le Goff A, Leroy J, Massoulié J, Bon S: Addition of a glycophosphatidylinositol to acetylcholinesterase. Processing, degradation, and secretion. J Biol Chem 2001;276:27881-27892.
47. Arpagaus M, Fedon Y, Cousin X, Chatonnet A, Bergé J-B, Fournier D, Toutant J-P: cDNA sequence, gene structure, and in vitro expression of ace-1, the gene encoding acetylcholinesterase of class A in the nematode Caenorhabditis elegans. J Biol Chem 1994;269:9957-9965.
48. Bon S, Massoulié J: Quaternary associations of acetylcholinesterase. 1. Oligomeric associations of T subunits with and without the amino-terminal domain of the collagen tail. J Biol Chem 1997;272:3007-3015.
49. Krejci E, Legay C, Thomine S, Sketelj J, Massoulié J: Differences in expression of acetylcholinesterase and collagen Q control the distribution and oligomerization of the collagen-tailed forms in fast and slow muscles. J Neurosci 1999;19:10672-10679.
50. Bon S, Rosenberry TL, Massoulié J: Amphiphilic, glycophosphatidylinositol-specific phospholipase C (PI-PLC)-insensitive monomers and dimers of acetylcholinesterase. Cell Mol Neurobiol 1991;11:157-172.
51. Giles K: Interactions underlying subunit association in cholinesterases. Protein Eng 1997;10:677-685.
52. Morel N, Leroy J, Ayon A, Massoulié J, Bon S: Acetylcholinesterase H and T dimers are associated through the same contact. Mutations at this interface interfere with the C-terminal T peptide, inducing degradation rather than secretion. J Biol Chem 2001;276:37379-37389.
53. Simon S, Krejci E, Massoulié J: A four-to-one association between peptide motifs: Four C-terminal domains from cholinesterase assemble with one proline-rich attachment domain (PRAD) in the secretory pathway. EMBO J 1998;17:6178-6187.
54. Duval N, Krejci E, Grassi J, Coussen F, Massoulié J, Bon S: Molecular architecture of acetylcholinesterase collagen-tailed forms; construction of a glycolipid-tailed tetramer. EMBO J 1992;11:3255-3261.
55. Bon S, Coussen F, Massoulié J: Quaternary associations of acetylcholinesterase. 2. The polyproline attachment domain of the collagen tail. J Biol Chem 1997;272:3016-3021.
56. Feng G, Krejci E, Molgo J, Cunningham JM, Massoulié J, Sanes JR: Genetic analysis of collagen Q: Roles in acetylcholinesterase and butyrylcholinesterase assembly and in synaptic structure and function. J Cell Biol 1999;144:1349-1360.
57. Krejci E, Coussen F, Duval N, Chatel JM, Legay C, Puype M, Vandekerckhove J, Cartaud J, Bon S, Massoulié J: Primary structure of a collagenic tail peptide of Torpedo acetyl-cholinesterase: Coexpression with catalytic subunit induces the production of collagen-tailed forms in transfected cells. EMBO J 1991;10:1285-1293.
58. Krejci E, Thomine S, Boschetti N, Legay C, Sketelj J, Massoulié J: The mammalian gene of acetylcholinesterase-associated collagen. J Biol Chem 1997;272:22840-22847.
59. Bon S, Cartaud J, Massoulié J: The dependence of acetylcholinesterase aggregation at low ionic strength upon a polyanionic component. Eur J Biochem 1978;85:1-14.
60. Peng HB, Xie H, Rossi SG, Rotundo RL: Acetylcholinesterase clustering at the neuromuscular junction involves perlecan and dystroglycan. J Cell Biol 1999;145:911-921.
61. Rossi SG, Rotundo RL: Transient interactions between collagen-tailed acetylcholinesterase and sulfated proteoglycans prior to immobilization in the extracellular matrix. J Biol Chem 1996;271:1979-1987.
62. Emmerling MR, Johnson CD, Mosher DF, Lipton BH, Lilien JE: Cross-linking and binding of fibronectin with asymmetric acetylcholinesterase. Biochemistry 1981;20:3242-3247.
63. Deprez P, Doss-Pepe E, Brodsky B, Inestrosa NC: Interaction of the collagen-like tail of asymmetric acetylcholinesterase with heparin depends on triple-helical conformation, sequence and stability. Biochem J 2000;350: 283-290.
64. Deprez P, Inestrosa NC: Two heparin-binding domains are present on the collagenic tail of asymmetric acetylcholinesterase. J Biol Chem 1995;270:11043-11046.
65. Sketelj J, Brzin M: Asymmetric molecular forms of acetylcholinesterase in mammalian skeletal muscles. J Neurosci Res 1985;14:95-103.
66. Gennari K, Brunner J, Brodbeck U: Tetrameric detergent-soluble acetylcholinesterase from human caudate nucleus: Subunit composition and number of active sites. J Neurochem 1987;49:12-18.
67. Inestrosa NC, Roberts WL, Marshall TL, Ro-senberry TL: Acetylcholinesterase from bovine caudate nucleus is attached to membranes by a novel subunit distinct from those of acetylcholinesterases in other tissues. J Biol Chem 1987;262:4441-4444.
68. Navaratnam DS, Fernando FS, Priddle JD, Giles K, Clegg SM, Pappin DJ, Craig I, Smith AD: Hydrophobic protein that copurifies with human brain acetylcholinesterase: Amino acid sequence, genomic organization, and chromosomal localization. J Neurochem 2000;74:2146-2153.
69. Perrier AL, Cousin X, Boschetti N, Haas R, Chatel JM, Bon S, Roberts WL, Pickett SR, Massoulié J, Rosenberry TL, Krejci E: Two distinct proteins are associated with tetrameric acetylcholinesterase on the cell surface. J Biol Chem 2000;275:34260-34265.
70. Perrier AL, Massoulié J, Krejci E: PRiMA: The membrane anchor of acetylcholinesterase in the brain. Neuron 2002;33:275-285.
71. Xie W, Stribley JA, Chatonnet A, Wilder PJ, Rizzino A, McComb RD, Taylor P, Hinrichs SH, Lockridge O: Postnatal developmental delay and supersensitivity to organophosphate in gene-targeted mice lacking acetylcholinesterase. J Pharmacol Exp Ther 2000;293:896-902.
72. Xie W, Wilder PJ, Stribley J, Chatonnet A, Rizzino A, Taylor P, Hinrichs SH, Lockridge O: Knockout of one acetylcholinesterase allele in the mouse. Chem Biol Interact 1999;119-120:289-299.
73. Li B, Stribley JA, Ticu A, Xie W, Schopfer LM, Hammond P, Brimijoin S, Hinrichs SH, Lockridge O: Abundant tissue butyrylcholinesterase and its possible function in the acetylcholinesterase knockout mouse. J Neurochem 2000;75:1320-1331.
74. Gisiger V, Stephens HR: Localization of the pool of G4 acetylcholinesterase characterizing fast muscles and its alteration in murine muscular dystrophy. J Neurosci Res 1988;19:62-78.
75. Gisiger V, Bélisle M, Gardiner PF: Acetylcholinesterase adaptation to voluntary wheel running is proportional to the volume of activity in fast, but not slow, rat hindlimb muscles. Eur J Neurosci 1994;6:673-680.
76. Gisiger V, Jasmin BJ, Sherker S, Gardiner PF: The pool of G4 acetylcholinesterase characterizing rodent fast muscles is differentially regulated by the predominant type, dynamic or tonic, of natural activity; in Massoulié J, Bacou F, Barnard EA, Chatonnet A, Doctor BP, Quinn DM (eds): Cholinesterases: Structure, Function, Mechanism, Genetics and Cell Biology. Washington, American Chemical Society, 1991.
77. Gisiger V, Sherker S, Gardiner PF: Swimming training increases the G4 acetylcholinesterase content of both fast ankle extensors and flexors. FEBS Lett 1991;278:271-273.
78. Jasmin BJ, Gisiger V: Regulation by exercise of the pool of G4 acetylcholinesterase characterizing fast muscles: Opposite effects of running training in antagonist muscles. J Neurosci 1990;10:1444-1454.
79. Oliver LJ, Chatel JM, Massoulié J, Vigny M, Vallette FM: Molecular forms of acetylcholinesterase in dystrophic (mdx) mouse tissues. Neuromuscul Disord 1992;2:87-97.
80. Soreq H, Seidman S: Acetylcholinesterase - new roles for an old actor. Nat Rev Neurosci 2001;2:294-302.
81. Descarries L: The hypothesis of an ambient level of acetylcholine in the central nervous system. J Physiol (Paris) 1998;92:215-220.
82. Alvarez A, Opazo C, Alarcon R, Garrido J, Inestrosa NC: Acetylcholinesterase promotes the aggregation of amyloid-beta-peptide fragments by forming a complex with the growing fibrils. J Mol Biol 1997;272:348-361.
83. Inestrosa NC, Alvarez A, Perez CA, Moreno RD, Vicente M, Linker C, Casanueva OI, Soto C, Garrido J: Acetylcholinesterase accelerates assembly of amyloid-beta-peptides into Alzheimer's fibrils: Possible role of the peripheral site of the enzyme. Neuron 1996;16:881-891.
84. Alvarez A, Alarcon R, Opazo C, Campos EO, Munoz FJ, Calderon FH, Dajas F, Gentry MK, Doctor BP, De Mello FG, Inestrosa NC: Stable complexes involving acetylcholinesterase and amyloid-beta peptide change the biochemical properties of the enzyme and increase the neurotoxicity of Alzheimer's fibrils. J Neurosci 1998;18:3213-3223.
85. Calderon FH, von Bernhardi R, De Ferrari G, Luza S, Aldunate R, Inestrosa NC: Toxic effects of acetylcholinesterase on neuronal and glial-like cells in vitro. Mol Psychiatry 1998;3:247-255.
86. Carson KA, Geula C, Mesulam MM: Electron microscopic localization of cholinesterase activity in Alzheimer brain tissue. Brain Res 1991;540:204-208.
87. Wright CI, Geula C, Mesulam MM: Protease inhibitors and indoleamines selectively inhibit cholinesterases in the histopathologic structures of Alzheimer disease. Proc Natl Acad Sci USA 1993;90:683-686.
88. Inestrosa NC, Alarcon R: Molecular interactions of acetylcholinesterase with senile plaques. J Physiol (Paris) 1998;92:341-344.
89. Ichtchenko K, Hata Y, Nguyen T, Ullrich B, Missler M, Moomaw C, Südhof TC: Neuroligin 1: A splice site-specific ligand for β-neurexins. Cell 1995;81:435-443.
90. 2+ binding in cell surface associations. Protein Sci 2000;9:180-185.
91. Layer PG: Cholinesterases preceding major tracts in vertebrate neurogenesis. Bioessays 1990;12:415-420.
92. Layer PG, Alber R, Rathjen FG: Sequential activation of butyrylcholinesterase in rostral half somites and acetylcholinesterase in moto-neurones and myotomes preceding growth of motor axons. Development 1988;102:387-396.
93. Jones SA, Holmes C, Budd TC, Greenfield SA: The effect of acetylcholinesterase on outgrowth of dopaminergic neurons in organotypic slice culture of rat mid-brain. Cell Tissue Res 1995;279:323-330.
94. Layer PG, Weikert T, Alber R: Cholinesterases regulate neurite growth of chick nerve cells in vitro by means of a non-enzymatic mechanism. Cell Tissue Res 1993;273:219-226.
95. Sharma KV, Bigbee JW: Acetylcholinesterase antibody treatment results in neurite detachment and reduced outgrowth from cultured neurons: Further evidence for a cell adhesive role for neuronal acetylcholinesterase. J Neurosci Res 1998;53:454-464.
96. Sharma KV, Koenigsberger C, Brimijoin S, Bigbee JW: Direct evidence for an adhesive function in the noncholinergic role of acetylcholinesterase in neurite outgrowth. J Neurosci Res 2001;63:165-175.
97. Sternfeld M, Ming G, Song H, Sela K, Timberg R, Poo M, Soreq H: Acetylcholinesterase enhances neurite growth and synapse development through alternative contributions of its hydrolytic capacity, core protein, and variable C termini. J Neurosci 1998;18:1240-1249.
98. Grisaru D, Deutsch V, Shapira M, Pick M, Sternfeld M, Melamed-Book N, Kaufer D, Galyam N, Gait MJ, Owen D, Lessing JB, Eldor A, Soreq H: ARP, a peptide derived from the stress-associated acetylcholinesterase variant, has hematopoietic growth promoting activities. Mol Med 2001;7:93-105.
99. Harel M, Bon S, Liu WQ, Dvir H, Belbeoc'h S, Vidal M, Garbay C, Silman I, Massoulié J, Sussman J, in preparation.