Acetylcholinesterase: C-terminal domains, molecular forms and functional localization

Journal of Physiology Paris

Volumn 92, Issue 3-4, 1998, Pages 183-190

  Massoulié, Jean ^a   Anselmet, Alain ^a   Bon, Suzanne ^a   Krejci, Eric ^a   Legay, Claire ^a   Morel, Nathalie ^a   Simon, Stéphanie ^a  

^a ECOLE NORMALE SUPÉRIEURE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCHOLINESTERASE; COLLAGEN; DIMER; GLYCOLIPID; OLIGOMER; PROLINE;

ANIMAL CELL; CARBOXY TERMINAL SEQUENCE; CHOLINERGIC SYNAPSE; CONFERENCE PAPER; ENZYME ANALYSIS; ENZYME LOCALIZATION; ENZYME SUBUNIT; NEUROMUSCULAR SYNAPSE; NONHUMAN; PROTEIN DOMAIN; PROTEIN PROCESSING; VERTEBRATE;

EID: 0032105344     PISSN: 09284257     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0928-4257(98)80007-7     Document Type: Conference Paper

References (59)

1. [1] Sussman J.L., 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 253 (1991) 872-879.
2. [2] Ollis D.L., Cheah E., Cygler M., Dijkstra B., Frolow F., Franken S.M., Harel M., Remington S.J., Silman I., Schrag J. et al., The alpha/beta hydrolase fold, Protein Eng. 5 (1992) 197-211.
3. [3] Massoulié J., Pezzementi L., Bon S., Krejci E., Vallette F.M., Molecular and cellular biology of cholinesterases, Prog. Neurosci. 41 (1993) 31-91
4. [4] Sikorav J.L., Duval N., Anselmet A., Bon S., Krejci E., Legay C., Osterlund M., Reimund B., Massoulié J., Complex alternative splicing of acetylcholinesterase transcripts in Torpedo electric organ; primary structure of the precursor of the glycolipid-anchored dimeric form, EMBO J. 7 (1988) 2983-2993.
5. [5] Legay C., Bon S., Massoulié J., Expression of a cDNA encoding the glycolipid-anchored form of rat acetylcholinesterase, FEBS Lett. 315 (1993) 163-166.
6. [6] Li Y., Camp S., Rachinsky T.L., Getman D., Taylor P., Gene structure of mammalian acetylcholinesterase. Alternative exons dictate tissue-specific expression, J. Biol. Chem. 266 (1991) 23083-23090.
7. [7] Cousin X., Hotelier T., Liévin P., Toutant J.P., Chatonnet A., A cholinesterase genes server (ESTHER): a database of cholinesterase-related sequences for multiple alignments, phylogeetic relationships, mutations and structural data retrieval, Nucleic Acids Res. 24 (1996) 132-136.
8. [8] Li Y., Camp S., Taylor P., Tissue-specific expression and alternative mRNA processing of the mammalian acetylcholinesterase gene, J. Biol. Chem. 268 (1993) 5790-5797.
9. [9] Legay C., Huchet M., Massoulié J., Changeux J.P., Developmental regulation of acetylcholinesterase transcripts in the mouse diaphragm: alternative splicing and focalization, Eur. J. Neurosci. 7 (1995) 1803-1809.
10. [10] Kaufer D., Friedman A., Seidman S., Soreq H., Acute stress facilitates long-lasting changes in cholinergic gene expression, Nature 393 (1998) 373-377.
11. [11] Fournier D., Karch F., Bride J.-M., Hall L.M.C., Bergé J.-B., Spierer P., Drosophila melanogaster acetylcholinesterase gene: structure, evolution and mutations, J. Mol. Biol. 210 (1990) 15-22.
12. [12] Bucht G., Hjalmarsson K., Residues in Torpedo californica acetylcholinesterase necessary for processing to a glycosyl phosphatidylinositol-anchored form, Biochim. Biophys. Acta 1292 (1996) 223-232.
13. [13] Roberts W.L., Doctor B.P., Foster J.D., Rosenberry T.L., Bovine brain acetylcholinesterase primary sequence involved in intersubunit disulfide linkages, J. Biol. Chem. 266 (1991) 7481-7487.
14. [14] Toutant J.-P., Insect acetylcholinesterase: catalytic properties, tissue distribution and molecular forms, Prog. Neurobiol. 32 (1988) 423-446.
15. [15] Schumacher M., Maulet Y., Camp S., Taylor P., Multiple messenger RNA species give rise to the structural diversity in acetylcholinesterase, J. Biol. Chem. 263 (1988) 18979-18987.
16. [16] 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. 269 (1994) 9957-9965.
17. [17] Schumacher M., Camp S., Maulet Y., Newton M., MacPhee-Quigley K., Taylor S.S., Friedmann T., Taylor P., Primary structure of Torpedo californica acetylcholinesterase deduced from its cDNA sequence, Nature 319 (1986) 407-409.
18. [18] Sikorav J.L., Krejci E., Massoulié J., cDNA sequences of Torpedo marmorata acetylcholinesterase: primary structure of the precursor of a catalytic subunit; existence of multiple 5′-untranslated regions, EMBO J. 6 (1987) 1865-1873.
19. [19] Simon S., Massoulié J., Cloning and expression of acetylcholinesterase from Electrophorus: splicing pattern of the 3′ exons in vivo and in transfected mammalian cells, J. Biol. Chem. 273 (1997) 33045-33055.
20. [20] 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 acetylcholinesterase in the snake liver and muscle, J. Biol. Chem. 273 (1998) 9812-9820.
21. [21] Anselmet A., Fauquet M., Chatel J.M., Maulet Y., Massoulié J., Vallette F.M., Evolution of acetylcholinesterase transcripts and molecular forms during development in the central nervous system of the quail, J. Neurochem. 62 (1994) 2158-2165.
22. [22] Legay C., Bon S., Vernier P., Coussen F., Massoulié J., Cloning and expression of a rat acetylcholinesterase subunit: generation of multiple molecular forms and complementarity with a Torpedo collagenic subunit, J. Neurochem. 60 (1993) 337-346.
23. [23] 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. 262 (1987) 549-557.
24. [24] Arpagaus M., Kott M., Vatsis K.P., Bartels C.F., La Du B.N., Lockridge O., Structure of the gene for human butyrylcholinesterase. Evidence for a single copy, Biochemistry 29 (1990) 124-131.
25. [25] Bon S., Rosenberry T.L., Massoulié J., Amphiphilic, glycophosphatidylinositol-specific phospholipase C (PI-PLC)-insensitive monomers and dimers of acetytcholinesterase, Cell. Mol. Neurobiol. 11 (1991) 157-172.
26. [26] Bon S., Massoulié J., Quaternary associations of acetylcholinesterase. I Oligomeric associations of T subunits with and without the amino-terminal domain of the collagen tail, J. Biol. Chem. 272 (1997) 3007-3015.
27. [27] Liao J., Boschetti N., Mortensen V., Jensen S.P., Koch C., Norgaard-Pedersen B., Brodbeck U., Characterization of salt-soluble forms of acetylcholinesterase from bovine brain, J. Neurochem. 63 (1994) 1446-1453.
28. [28] Krejci E., Coussen F., Duval N., Chatel J.M., Legay C., Puype M., Vandekerckhove J., Cartaud J., Bon S., Massoulié J., Primary structure of a collagenic tail peptide of Torpedo acetylcholinesterase: co-expression with catalytic subunit induces the production of collagen-tailed forms in transfected cells, EMBO J. 10 (1991) 1285-1293.
29. [29] Krejci E., Thomine S., Boschetti N., Legay C., Sketelj J., Massoulié J., The mammalian gene of acetylcholinesterase-associated collagen, J. Biol. Chem. 272 (1997) 22840-22847.
30. [30] Gennari K., Brunner J., Brodbeck U., Tetrameric detergent-soluble acetylcholinesterase from human caudate nucleus: subunit composition and number of active sites, J. Neurochem. 49 (1987) 12-18.
31. [31] Inestrosa N.C., Roberts W.L., Marshall T.L., Rosenberry T.L., Acetylcholinesterase from bovine caudate nucleus is attached to membranes by a novel subunit distinct from those of acetylcholinesterases in other tissues, J. Biol. Chem. 262 (1987) 4441-4444.
32. [32] Boschetti N., Liao J., Brodbeck U., The membrane form of acetylcholinesterase from rat brain contains a 20 kDa hydrophobic anchor, Neurochem. Res. 19 (1994) 359-365.
33. [33] Boschetti N., Brodbeck U., The membrane anchor of mammalian brain acetylcholinesterase consists of a single glycosylated protein of 22 kDa, FEBS Lett. 380 (1996) 133-136.
34. [34] 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. 271 (1996) 15099-15108.
35. [35] 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. 387 (1996) 196-200.
36. [36] Bourguet D., Raymond M., Fournier D., Malcolm C.A., Toutant J.-P., Arpagaus M., Existence of two acetylcholinesterase in the mosquito Culex pipiens (Diptera: Culicidae), J. Neurochem. 67 (1996) 2115-2123.
37. [37] Sutherland D., McClellan D.S., Milner D., Soong W., Axon N., Sanders M., Hester A., Kao Y.-H., Poczatek T., Routt S., Pezzementi L., Two cholinesterase activities and genes are present in amphioxus, J. Exp. Zool. 277 (1997) 213-229.
38. [38] Grauso M., Culetto E., Combes D., Fedon Y., Toutant J.-P., Arpagaus M., Existence of four acetylcholinesterase genes in the nematodes Caenorhabditis elegans and Caenorhabditis briggsae, FEBS Lett. 424 (1998) 279-284.
39. [39] 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 89 (1992) 10827-10831.
40. [40] Bertrand C., Takke C., Cousin X., Toutant J.P., Chatonnet A., in: Zebrafish development and genetics, Cold Spring Harbor, 1996, 105 p.
41. [41] Toutant J.P., Massoulié J., Cholinesterases: tissue and cellular distribution of molecular forms and their physiological regulation, Handb. Exp. Pharmacol. 86 (1988) 225-265.
42. [42] Duval N., Massoulié J., Bon S., H and T subunits of acetylcholinesterase from Torpedo, expressed in COS cells, generate all types of globular forms, J. Cell Biol. 118 (1992) 641-653.
43. [43] Kodukula K., Gerber L.D., Amthauer R., Brink L., Udenfriend S., Biosynthesis of glycosylphosphatidylinositol (GPI)anchored membrane proteins in intact cells: specific amino acid requirements adjacent to the site of cleavage and GPI attachment, J. Cell Biol. 120 (1993) 657-664.
44. [44] Moran P., Caras I.W., Requirements for glycophosphatidylinositol attachment are similar but not identical in mammalian cells and parasitic protozoa, J. Cell Biol. 125 (1994) 333-343.
45. [45] Lapidot-Lifson Y., Prody C.A., Ginzberg D., Meytes D., Zakut H., Soreq H., Coamplification of human acetylcholinesterase and butyrylcholinesterase genes in blood cells: correlation with various leukemias and abnormal megakaryocytopoiesis, Proc. Natl. Acad. Sci. USA 86 (1989) 4715-4719.
46. [46] Patinkin D., Seidman S., Eckstein F., Benseler F., Zakut H., Soreq H., Manipulations of cholinesterase gene expression modulate murine megakaryocytopoiesis in vitro, Mol. Cell. Biol. 10 (1990) 6046-6050.
47. [47] Giles K., Interactions underlying subunit association in cholinesterases, Protein Eng. 10 (1997) 677-685.
48. [48] Bon S., Toutant J.P., Méflah K., Massoulié J., Amphiphilic and nonamphiphilic forms of Torpedo cholinesterases: I. Solubility and aggregation properties, J. Neurochem. 51 (1988) 776-785.
49. [49] Bon S., Toutant J.P., Méflah K., Massoulié J., Amphiphilic and nonamphiphilic forms of Torpedo cholinesterases: II. Electrophoretic variants and phosphatidylinositol phospholipase C-sensitive and -insensitive forms, J. Neurochem. 51 (1988) 786-794.
50. [50] Massoulié J., Sussman J., Bon S., Silman I., Structure and functions of acetytcholinesterase and butyrylcholinesterase, Prog. Brain Res. 98 (1993) 139-146.
51. [51] Lazar M., Salmeron E., Vigny M., Massoulié J,. Heavy isotope-labeling study of the metabolism of monomeric and tetrameric acetylcholinesterase forms in the murine neuronal-like T 28 hybrid cell line, J. Biol. Chem. 259 (1984) 3703-3713.
52. [52] Bon S., Coussen F., Massoulié J., Quaternary associations of acetylcholinesterase; II. the polyproline attachment domain of the collagen tail, J. Biol. Chem. 272 (1997) 3016-3021.
53. [53] Tsim K.W., Randall W.R., Barnard E.A., An asymmetric form of muscle acetylcholinesterase contains three subunit types and two enzymic activities in one molecule, Proc. Natl. Acad. Sci. USA 85 (1988) 1262-1266.
54. [54] Chan D.C., Bedford M.T., Leder P., Formin binding proteins bear WWP/WW domains that bind proline-rich peptides and functionally resemble SH3 domains, EMBO J. 15 (1996) 1045-1054.
55. [55] Massoulié J., Sussman J.L., Doctor B.P., Soreq H., Velan B., Cygler M., Rotundo R.L., Shafferman A., Silman I., Taylor P., in: Shafferman A., Velan B. (Eds.), Multidisciplinary approaches to cholinesterase functions, Plenum Press, New York, 1992, pp. 285-288.
56. [56] Hutchinson D.O., Engel A.G., Walls T.J., Nakano S., Camp S., Taylor P., Harper C.M., Brengman J.M., The spectrum of congenital end-plate acetylcholinesterase deficiency, Ann. N.Y. Acad. Sci. 21 (1993) 469-486.
57. [57] Camp S., Bon S., Li Y., Getman D.K., Engel A.C., Massoulié J., Taylor P., Patients with congenital myasthenia associated with end-plate acetylcholinesterase deficiency show normal sequence, mRNA splicing, and assembly of catalytic subunits, J. Clin. Invest. 95 (1995) 333-340.
58. [58] Rossi S.G., Rotundo R.L., Transient interactions between collagen-tailed acetylcholinesterase and sulfated proteoglycans prior to immobilization ion the extracellular matrix, J. Biol. Chem. 271 (1996) 1979-1987.
59. [59] Gisiger V., Bélisle M., Gardiner P.F., Acetylcholinesterase adaptation to voluntary wheel running is proportional to the volume of activity in fast, but not slow, rat hindlimb muscles, Eur. J. Neurosci. 6 (1994) 673-680.