Why so many forms of acetylcholinesterase?

Microscopy Research and Technique

Volumn 49, Issue 1, 2000, Pages 56-72

  Legay, Claire ^a  

^a ECOLE NORMALE SUPÉRIEURE   (France)

Author keywords

Acetylcholinesterase; Alternative splicing; ColQ; Myopathies; Neuromuscular junction

Indexed keywords

ENZYMES; MAMMALS;

ACETYLCHOLINE RECEPTOR; ACETYLCHOLINESTERASE; ALTERNATIVE SPLICING; BASAL LAMINA; COLQ; MYOPATHY; NEUROMUSCULAR JUNCTIONS; PRESYNAPTIC; SUB-CELLULAR; TISSUE SPECIFICS;

CATALYST ACTIVITY;

ACETYLCHOLINESTERASE;

ANIMAL CELL; ARTICLE; CELLULAR DISTRIBUTION; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME ASSAY; ENZYME MECHANISM; ENZYME POLYMORPHISM; ENZYME STRUCTURE; NEUROMUSCULAR SYNAPSE; NONHUMAN; PRIORITY JOURNAL; TORPEDO;

ANIMALIA; MAMMALIA;

EID: 0034176868     PISSN: 1059910X     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-0029(20000401)49:1<56::AID-JEMT7>3.0.CO;2-R     Document Type: Article

References (166)

1. Adler M, Filbert MG. 1990. Role of butyrylcholinesterase in canine tracheal smooth muscle function. FEBS Lett 267:107-110.
2. Allemand P, Bon S, Massoulié J, Vigny M. 1981. The quaternary structure of chicken acetylcholinesterase and butyrylcholinesterase; effect of collagenase and trypsin. J. Neurochem 36:860-867.
3. Anglister L. 1991. Acetylcholinesterase from the motor nerve terminal accumulates on the synaptic basal lamina of the myofiber. J Cell Biol 115:755-764.
4. Anglister L, Stiles JR, Salpeter MM. 1994. Acetylcholinesterase density and turnover number at frog neuromuscular junctions, with modeling of their role in synaptic function. Neuron 12:783-794.
5. Anglister L, Eichler J, Szabo M, Haesaert B, Salpeter MM. 1998. 1251-labeled fasciculin 2: a new tool for quantitation of acetylcholinesterase densities at synaptic sites by EM-autoradiography. J Neurosci Methods 81:63-71.
6. Atanasova E, Chiappa S, Wieben E, Brimijoin S. 1999, Novel messenger RNA and alternative promoter for murine acetylcholinesterase. J Biol Chem 274:21078-21084.
7. Bacou F, Vigneron P, Massoulié J. 1982. Acetylcholinesterase forms in fast and slow rabbit muscle. Nature 296:661-664.
8. Ben Aziz-Aloya R, Sternfeld M, Soreq H. 1993. Promoter elements and alternative splicing in the human ACHE gene. Prog Brain Res 98:147-153.
9. Bevan S, Steinbach JH. 1977. The distribution of alpha-bungarotoxin binding sites of mammalian skeletal muscle developing in vivo. J Physiol (London) 267:195-213.
10. Bon S, Massoulié J. 1997. Quaternary associations of acetylcholinesterase. I. Oligomeric associations of T subunits with and without the ammo-terminal domain of the collagen tail. J Biol Chem 272: 3007-3015.
11. Bon S, Cartaud J, Massoulié J. 1978. The dependence of acetylcholinesterase aggregation at low ionic strength upon a polyanionic component. Eur J Biochem 85:1-14.
12. Bon S, Méflah K, Mussel F, Grassi J, Massoulié J. 1987. An immunoglobulin M monoclonal antibody, recognizing a subset of acetylcholinesterase molecules from electric organs of Electrophorus and Torpedo, belongs to the HNK-1 anti-carbohydrate family. J Neurochem 49:1720-1731.
13. Bon S, Coussen F, Massoulié J. 1997. Quaternary associations of acetylcholinesterase; II. the polyproline attachment domain of the collagen tail. J Biol Chem 272:3016-3021.
14. Boudreau-Larivière C, Jasmin BJ. 1999. Calcitonin gene-related peptide decreases expression of acetylcholinesterase in mammalian myotubes. FEBS Lett 444:22-26.
15. Boudreau-Larivière C, Gisiger V, Michel RN, Hubatsch DA, Jasmin BJ. 1997. Fast and slow skeletal muscles express a common basic profile of acetylcholinesterase molecular forms. Am J Physiol 272: 68-76.
16. Brandan E, Inestrosa NC. 1984. Binding of asymmetric forms of acetylcholinesterase to heparin. Biochem J 221:415-422.
17. Brandan E, Maldonado M, Garrido J, Inestrosa NC. 1985. Anchorage of collagen-tailed acetylcholinesterase to the extracellular matrix is mediated by heparan sulfate proteoglycans. J Cell Biol 101:985-992.
18. Brimijoin S. 1979. Axonal transport and subcellular distribution of molecular forms of acetylcholinesterase in rabbit sciatic nerve. Mol Pharmacol 15:641-648.
19. Brockman SK, Usiak MF, Younkin SG. 1986. Assembly of monomeric acetylcholinesterase into tetrameric and asymmetric forms. J Biol Chem 261:1201-1207.
20. Brzin M, Sketelj J, Tennyson VM, Kiauta T, Budininkas-Schoenebeck M. 1981. Activity, molecular forms, and cytochemistry of cholinesterases in developing rat diaphragm. Muscle Nerve 4:505-513.
21. Camp S, Bon S, Li Y, Getman DK, Engel AG, Massoulié J, Taylor P. 1995. Patients with congenital myasthenia associated with endplate acetylcholinesterase deficiency show normal sequence, mRNA splicing and assembly of catalytic subunits. J Clin Invest 95:333-340.
22. Chan RY, Adatia FA, Krupa AM, Jasmin BJ. 1998. Increased expression of acetylcholinesterase T and R transcripts during hematopoietic differentiation is accompanied by parallel elevations in the levels of their respective molecular forms. J Biol Chem 273:9727-9733.
23. Chan RY, Boudreau-Larivière C, Angus LM, Mankal FA, Jasmin BJ. 1999. An intronic enhancer containing an N-box motif is required for synapse-and tissue-specific expression of the acetylcholinesterase gene in skeletal muscle fibers. Proc Natl Acad Sci USA 96:4627-4632.
24. Collins PL, Younkin SG. 1982. Effect of denervation on the molecular forms of acetylcholinesterase in rat diaphragm. J Biol Chem 257: 13638-13644.
25. Côté P, Moukhles H, Lindenbaum M, Carbonetto S. 1999. Chimeric mice deficient in dystroglycans develop muscular dystrophy and have disrupted myoneural synapses. Nature Genet 23:338-342.
26. Couraud JY, Di Giamberardino L. 1980. Axonal transport of the molecular forms of acetylcholinesterase in chick sciatic nerve. J Neurochem 35:1053-1066.
27. Cousin X, Bon S, Massoulié J, Bon C. 1998. 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 273:9812-9820.
28. Cresnar B, Çrne-Finderle N, Breskvar K, Sketelj J. 1994. Neural regulation of muscle acetylcholinesterase is exerted on the level of its mRNA. J Neurosci Res 38:294-299.
29. Dale H.H. 1914. The action of certain esters of choline and their relation to muscarine. J Pharmacol Exp Ther 6:147-190.
30. De La Porte S, Vallette FM, Grassi J, Vigny M, Koenig J. 1986. Presynaptic or postsynaptic origin of acetylcholinesterase at neuromuscular junctions? An immunological study in heterotogous nerve-muscle cultures. Dev Biol 116:69-77.
31. De La Porte S, Chaubourt E, Fabre F, Poulas K, Chapron J, Eymard B, Tzartos S, Koenig J. 1998. Accumulation of acetylcholine receptors is a necessary condition for normal accumulation of acetylcholinesterase during in vitro neuromuscular synaptogenesis. Eur J Neurosci 10:1631-1643.
32. DeChiara TM, Bowen DC, Valenzuela DM, Simmons MV, Poueymirou WT, Thomas S, Kinetz E, Compton DL, Rojas E, Park JS, Smith C, DiStephano PS, Glass DJ, Burden SJ, Yancopoulos GD. 1996. The receptor tyrosine kinase MuSK is required for neuromuscular junction formation in vivo. Cell 85501-512.
33. Deconinck AE, Potter AC, Tinsley JM, Wood SJ, Vater R, Young C, Metzinger L, Vincent A, Slater CR, Davies KE. 1997a. Postsynaptic abnormalities at the neuromuscular junctions of utrophin-deficient mice. J Cell Biol 136:883-894.
34. Deconinck AE, Rafael JA, Skinner JA, Brown SC, Potter AC, Metzinger L, Watt DJ, Dickson JG, Tinsley JM, Davies KE. 1997b. Utrophin-dystrophin-deficient mice as a model for Duchenne muscular dystrophy. Cell 90:717-727.
35. Deprez P, Inestrosa NC. 1995. Two heparin-binding domains are present on the collagenic tail of asymmetric acetylcholinesterase. J Biol Chem 270:11043-11046.
36. Doctor BP, Chapman TC, Christner CE, Deal CD, De La Hoz DM, Gentry MK, Ogert RA, Rush RS, Smyth KK, Wolfe AD. 1990. Complete amino acid sequence of fetal bovine serum acetylcholinesterase and its comparison in various regions with other cholinesterases. FEBS Lett 266:123-127.
37. Donger C, Krejci E, Pou Serradell A, Eymard B, Bon S, Nicole S, Chateau D, Gary F, Fardeau M, Massoulié J, Guicheney P. 1998. Mutation in the human acetylcholinesterase-associated collagen gene Co1Q, is responsible for congenital myasthenic syndrome with end-plate acetylcholinesterase deficiency (type Ic). Am J Human Genet 63:967-975.
38. Duclert A, Changeux JP. 1995. Acetylcholine receptor gene expression at the developing neuromuscular junction. Physiol Rev 75:339-368.
39. Ehrlich G, Viegas-Pequignot E, Ginzberg D, Sindel L, Soreq H, Zakut H. 1992. Mapping the human acetylcholinesterase gene to chromosome 7q22 by fluorescent in situ hybridization coupled with selective PCR amplification from a somatic hybrid cell panel and chromosome-sorted DNA libraries. Genomics 13:1192-197.
40. Engel AG, Lambert EH, Gomez MR. 1977. A new myasthenic syndrome with end-plate acetylcholinesterase deficiency, small nerve terminals, and reduced acetylcholine release. Ann Neurol 1:315-330.
41. Fambrough DM. 1979. Control of acetylcholine receptors in skeletal muscle. Physiol Rev 59:165-227.
42. Feng G, Krejci E, Molgo J, Cunningham JM, Massoulié J, Sanes JR. 1999. Genetic analysis of Collagen Q: Roles in acetylcholinesterase and butyrylcholinesterase assembly and in synaptic structure and function. J Cell Biol 144:1349-1360.
43. Fernandas KJ, Kobayashi NR, Jasmin BJ, Tetzlaff W. 1998. Acetylcholinesterase gene expression in axotomized rat facial motoneurons is differentially regulated by neurotrophins: correlation with trkB and trkC mRNA levels and isoforms. J Neurosci 18:9936-9947.
44. Fernandez HL, Donoso JA. 1988. Exercise selectively increases G4 AChE activity in fast-twitch muscle. J Appl Physiol 65:2245-2252.
45. Fernandez HL, Hodges-Savola CA. 1996. Physiological regulation of G4 AChe in fast-twitch muscle: effects of exercise and CGRP. J Appl Physiol 80:357-362.
46. Fernandez HL, Duell MJ, Festoff BW. 1980. Bidirectional axonal transport of 16S acetylcholinesterase in rat sciatic nerve. J Neurobiol 11:31-39.
47. Fernandez HL, Singer PA, Mehler S. 1981. Retrograde axonal transport mediates the onset of regenerative changes in the hypoglossal nucleus. Neurosci Lett 25:7-11.
48. Fischbach GD, Frank E, Jessell TM, Rubin LL, Schuetze SM. 1978. Accumulation of acetylcholine receptors and acetylcholinesterase at newly formed nerve-muscle synapses. Pharmacol Rev 30:411-428.
49. Fuentes ME, Taylor P. 1993. Control of acetylcholinesterase gene expression during myogenesis. Neuron 10:679-687.
50. Gautam M, Noakes PG, Mudd J, Nichol M, Chu GC, Sanes JR, Merlie JP. 1995. Failure of postsynaptic specialization to develop at neuromuscular junctions of rapsyn-deficient mice. Nature 377:232-236.
51. Gautam M, Noakes PG, Moscoso L, Rupp F, Scheller RH, Merlie JP, Sanes JR. 1996. Defective neuromuscular synaptogenesis in agrin-deficient mutant mice. Cell 85:525-535.
52. Getman DK, Eubanks JH, Camp S, Evans GA, Taylor P. 1992. The human gene encoding acetylcholinesterase is located on the long arm of chromosome 7. Am J Hum Genet 51:170-177.
53. Getman DK, Mutero A, Inoue K, Taylor P. 1995. Transcription factor repression and activation of the human acetylcholinesterase gene. J Biol Chem 270:23511-23519.
54. Gibney G, Taylor P. 1990. Biosynthesis of Torpedo acetylcholinesterase in mammalian cells. Functional expression and mutagenesis of the glycophospholipid-anchored form. J Biol Chem 265:12576-12583.
55. Gilmour BP, Fanger GR, Newton C, Evans SM, Gardner PD. 1991. Multiple binding sites for myogenic regulatory factors are required for expression of the acetylcholine receptor gamma-subunit gene. J Biol Chem 266:19871-19874.
56. Gisiger V, Stephens HR. 1982. Acetylcholinesterase content in both motor nerve and muscle is correlated with twitch properties. Neurosci Lett 31:301-305.
57. Gisiger V, Bélisle M, Gardiner PF. 1994. Acetylcholinesterase adaptation to voluntary wheel running is proportional to the volume of activity in fast, but not slow, rat hindlimb muscles. Eur J Neurosci 6:673-680.
58. Grady RM, Merlie JP, Sanes JR. 1997a. Subtle neuromuscular defects in utrophin-deficient mice. J Cell Biol, 136, 871-882.
59. Grady RM, Teng H, Nichol MC, Cunningham JC, Wilkinson RS, Sanes JR. 1997b. Skeletal and cardiac myopathies in mice lacking utrophin and dystrophin: a model for Duchenne muscular dystrophy. Cell 90:729-738.
60. Grassi J, Vigny M, Massoulié J. 1982. Molecular forms of acetylcholinesterase in bovine caudate nucleus and superior cervical ganglion: solubility properties and hydrophobic character. J Neurochem 38:457-469.
61. Hall ZW. 1973. Multiple forms of acetylcholinesterase and their distribution in endplate and non-endplate regions of rat diaphragm muscle. J Neurol 4:343-361.
62. Hall ZW, Kelly RB. 1971. Enzymatic detachment of endplate acetylcholineterase from muscle. Nature New Biol 232:62-64.
63. Hall ZW Sanes JR. 1993. Synaptic structure and development: the neuromuscular junction. Cell 72/Neuron 10:99-121.
64. Harel M, Sussman JL, Krejci E, Bon S, Chanal P, Massoulié J, Silman I. 1992. Conversion of acetylcholinesterase to butyrylcholinesterase: modeling and mutagenesis. Proc Natl Acad Sci USA 89:10827-10831.
65. Hutchinson DO, Walls TJ, Nakano S, Camp S, Taylor P, Harper CM, Groover RV, Peterson HA, Jamieson DG, Engel AG. 1993. Congenital end-plate acetylcholinesterase deficiency. Brain 116:633-653.
66. Incardona JP, Rosenberry TL. 1996. Replacement of the glycoinositol phospholipid anchor of Drosophila acetylcholinesterase with a transmembrane domain does not alter sorting in neurons and epithelia but results in behavioral defects. Mol Biol Cell 7:613-630.
67. Jasmin BJ, Gisiger V. 1990. Regulation by exercise of the pool of G4 acetylcholinesterase characterizing fast muscles: opposite effects of running training in antagonist muscles. J Neurosci 10:1444-1454.
68. Jasmin BJ, Lee RK, Rotundo RL. 1993. Compartmentalization of acetylcholinesterase mRNA and enzyme at the vertebrate neuromuscular junction. Neuron 11:467-477.
69. Kaufer D, Friedman A, Seidman S, Soreq H. 1998. Acute stress facilitates long-lasting changes in cholinergic gene expression. Nature 393:373-377.
70. Kerem A, Kronman C, Bar-Nun S, Shafferman A, Velan B. 1993. Interrelations between assembly and secretion of recombinant human acetylcholinesterase. J Biol Chem 268:180-184.
71. Koenig J, Vigny M. 1978. Neural induction of the 16S acetylcholinesterase in muscle cell cultures. Nature 271:75-77.
72. Krejci E, Coussen F, Duval N, Chatel JM, Legay C, Puype M, Vandekerckhove J, Cartaud J, Bon S, Massoulié J. 1991. 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 10:1285-1293.
73. Krejci E, Thomine S, Boschetti N, Legay C, Sketelj J, Massoulié J. 1997. The mammalian gene of acetylcholinesterase-associated collagen. J Biol Chem 272:22840-22847.
74. Krejci E, Legay C, Thomine S, Sketelj J, Massoulié J. 1999. 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 19:10672-10679.
75. Kronman C, Velan B, Gozes Y, Leitner M, Flashner Y, Lazar A, Marcus D, Sery T, Papier Y, Grosfeld H, Cohen S, Shafferman A. 1992. Production and secretion of high levels of recombinant human acetylcholinesterase in cultured cell lines: microheterogeneity of the catalytic subunit. Gene 121:295-304.
76. Kronman C, Velan B, Marcus D, Ordentlich A, Reuveny S, Shafferman A. 1995. Involvement of oligomerization N-glycosylation and sialylation in the clearance of cholinesterases from the circulation. Biochem J 311:959-967.
77. Lai J, Jedrzejczyk J, Pizzey JA, Green D, Barnard EA. 1986. Neural control of the forms of acetylcholinesterase in slow mammalian muscles. Nature 321:72-74.
78. Layer PG, Willbold E. 1995. Novel functions of cholinesterases in development, physiology and disease. Prog Histochem Cytochem 29:1-99.
79. Lazar M, Salmeron E, Vigny M, Massoulié J. 1984. Heavy isotope-labeling study of the metabolism of monomeric and tetrameric acetylcholinesterase forms in the murine neuronal-like T28 hybrid cell line. J Biol Chem 259:3703-3713.
80. Legay C, Bon S, Massoulíe J. 1993a. Expression of a cDNA encoding the glycolipid-anchored form of rat acetylcholinesterase. FEBS Lett 315:163-166.
81. Legay C, Bon S, Vernier P, Coussen F, Massoulié J. 1993b. Cloning and expression of a rat acetylcholinesterase subunit: generation of multiple molecular forms and complementarity with a Torpedo collagenic subunit. J Neurochem 60:337-346.
82. Legay C, Huchet M, Massoulié J, Changeux JP. 1995. Developmental regulation of acetylcholinesterase transcripts in the mouse diaphragm: alternative splicing and focalization. Eur J Neurosci 7:1803-1809.
83. Legay C, Mankal FA, Massoulié J, Jasmin BJ. 1999. Stability and secretion of acetylcholinesterase forms in skeletal muscle cells. J Neurosci 19:8252-8259.
84. Lev-Lehman E, Ginzberg D, Hornreich G, Ehrlich G, Meshorer A, Eckstern F, Soreq H, Zakut H. 1994. Antisense inhibition of acetylcholinesterase gene expression causes transient hematopoietic alterations in vivo. Gene Ther 1:127-135.
85. Li Y, Camp S, Rachinsky TL, Bongiorno C, Taylor P. 1993a. Promoter elements and transcriptional control of the mouse acetylcholinesterase gene. J Biol Chem 268:3563-3572.
86. Li Y, Camp S, Taylor P. 1993b. Tissue-specific expression and alternative mRNA processing of the mammalian acetylcholinesterase gene. J Biol Chem 268:5790-5797.
87. Li Y, Camp S, Rachinsky TL, Getman D, Taylor P. 1991. Gene structure of mammalian acetylcholinesterase. Alternative exons dictate tissue-specific expression. J Biol Chem 266:23083-23090.
88. Liao J, Heider H, Sun MC, Brodbeck U. 1992. Different glycosylation in acetylcholinesterases from mammalian brain and erythrocytes. J Neurochem 58:1230-1238.
89. Lømo T, Slater CR. 1980. Acetylcholine sensitivity of developing ectopic nerve-muscle junctions in adult rat soleus muscles. J Physiol (London) 303:173-189.
90. Lømo T, Massoulie J, Vigny M. 1985. Stimulation of denervated rat soleus muscle with fast and slow activity patterns induces different expression of acetylcholinesterase molecular forms. J Neurosci 5:1180-1187.
91. Luo Z, Fuentes ME, Taylor P. 1994. Regulation of acetylcholinesterase mRNA stability by calcium during differentiation from myoblasts to myotubes. J Biol Chem 269:27216-27223.
92. Luo ZD, Camp S, Mutero A, Taylor P. 1998. Splicing of 5' introns dictates alternative splice selection of acetylcholinesterase pre-mRNA and specific expression during myogenesis. J Biol Chem 273:28486-28495.
93. Massoulié J, Sussman JL, Doctor BP, Soreq H, Velan B, Cygler M, Rotunda RL, Shafferman A, Silman I, Taylor P. 1992. Recommendations for nomenclature in cholinesterases. In Shafferman A, Velan B, editors. Multidisciplinary approaches to cholinesterase functions. New York: Plenum Press, p 285-288.
94. Massoulié J, Pezzementi L, Bon S, Krejci E, Valletta JM. 1993. Molecular and cellular biology of cholinesterases. Progr Neurobiol 41: 31-91.
95. Massoulié J Anselmet A, Bon S, Krejci E, Legay C, Morel N, et Simon S. 1998. Acetylcholinesterase: C-terminal domains, molecular forms and functional localization. J Physiol 92:183-190.
96. Maulet Y, Camp S, Gibney G, Rachinsky TL, Ekstrom TJ, Taylor P. 1990. Single gene encodes glycophospholipid-anchored and asymmetric acetylcholinesterase forms: alternative coding exons contain inverted repeat sequences. Neuron 4:289-301.
97. McMahan UJ, Sanes JR, Marshall LM. 1978. Cholinesterase is associated with the basal lamina at the neuromuscular junction. Nature 271:172-174.
98. Méflah K, Bernard S, Massoulié J. 1984. Interactions with lectins indicate differences in the carbohydrate composition of the membrane-bound enzymes acetylcholinesterase and 5'- nucleotidase in different cell types. Biochimie 66:59-69.
99. Meier T, Wallace BG. 1998. Formation of the neuromuscular junction: molecules and mechanisms. Bioessays 20:819-829.
100. Mendel B, Rudney H. 1943. Cholinesterase. 3. Specific tests for true cholinesterase and pseudo-cholinesterase. Biochem J 37:473-476.
101. Michel RN, Vu CQ, Tetzlaff W, Jasmin BJ. 1994. Neural regulation of acetylcholinesterase mRNAs at mammalian neuromuscvular synapses. J Cell Biol 127:1061-1069.
102. Missias AC, Mudd J, Cunningham JM. Steinbach JH, Merlie JP, Sanes JR. 1997. Development 124:5075-5086.
103. Moody-Corbett F, Cohen MW. 1981. Localization of cholinesterase at sites of high acetylcholine receptor density on embryonic amphibian muscle cells cultured without nerve. J Neurosci 1:596-605.
104. Mutero A, Camp S, Taylor P. 1995. Promoter elements of the mouse acetylcholinesterase gene. Transcriptional regulation during muscle differentiation. J Biol Chem 270:1866-1872.
105. Noakes PG, Gautam M, Mudd J, Sanes JR, Merlie JP. 1995. Aberrant differentiation of neuromuscular junctions in mice lacking s-laminin/ laminin β2. Nature 374:258-262.
106. Ohno K, Brengman J, Tsujino A, Engel AG. 1998. Human endplate acetylcholinesterase deficiency caused by mutations in the collagen-like (Co1Q) of the asymmetric enzyme. Proc Natl Acad Sci USA 95:9654-9659.
107. Ohno K, Brengman JM, Felice KJ, Cornblath DR, Engel AW. 1999. Congenital end-plate acetylcholinesterase deficiency caused by a nonsense mutation and an A→G splice-donor-site mutation at position +3 of the collagen-tail-subunit gene (COLQ): how does G at position +3 result in aberrant splicing? Am J Hum Genet 65:635-644.
108. Paoletti P, Mocali A, Vannucchi AM. 1992. Acetylcholinesterase in murine erythroleukemia (Friend) cells: avidence for megakaryocyte-like expression and potential growth-regulatory role of enzyme activity. Blood 79:2873-2879.
109. Peng HB, Ali AA, Daggett DF, Rauvala H, Hassell JR, Smalheiser NR. 1998. The relationship between perlecan and dystroglycan and its implication in the formation of the neuromuscular junction. Cell Adhes Commun 5:475-489.
110. Peng HB, Xie H, Rossi SG, Rotundo RL. 1999. Acetylcholinesterase clustering at the neuromuscular junction involves perlecan and dystroglycan. J Cell Biol 145:911-921.
111. Prives J, Silman I, Amsterdam A. 1976. Appearance and disappearance of acetylcholine receptor during differentiation of chick skeletal muscle in vitro. Cell 7:543-550.
112. Prockop DJ, Kivirikko KI. 1995. Collagens: molecular biology, diseases and potentials for therapy. Annu Rev Biochem 64:403-434.
113. Rachinsky TL, Camp S, Li Y, Ekstrom TJ, Newton M, Taylor P. 1990. Molecular cloning of mouse acetylcholinesterase: tissue distribution of alternatively spliced mRNA species. Neuron 5: 317-327.
114. Rachinsky TL, Crenshaw E, Taylor P. 1992. Assignment of the gene for acetylcholinesterase to distal mouse chromosome 5. Genomics 14:511-514.
115. Rakonczay Z, Vincendon G, Zanetta JP. 1981. Heterogeneity of rat brain acetylcholinesterase: a study by gel filtration and gradient centrifugation. J Neurochem 37:662-669.
116. Randall WR, Rimer M, Gough NR. 1994. Cloning and analysis of chicken acetylcholinesterase transcripts from muscle and brain. Biochim Biophys Acta 1218:453-456.
117. Rieger F, Vigny M. 1976. Solubilization and physicochemical characterization of rat brain acetylcholinesterase: development and maturation of its molecular forms. J Neurochem 27:121-129.
118. Rieger F, Koenig J, Vigny M. 1980. Spontaneous contractile activity and the presence of the 16S form of acetylcholinesterase in rat muscle cells in culture. Reversible suppressive action of tetrodotoxin. Dev Biol 76:358-365.
119. Rodriguez-Borrajo C, Barat A, Ramirez G. 1982. Solubilization of collagen-tailed molecular forms of acetylcholinesterase from several brain areas in different vertebrate species. Neurochem Int 4:563-568.
120. Rossi SG, Rotundo RL. 1992. Cell surface acetylcholinesterase molecules on multinucleated myotubes are clustered over the nucleus of origin. J Cell Biol 119:1657-1667.
121. Rossi SG, Rotundo RL. 1993. Localization of "non-extractible" acetylcholinesterase to the vertebrate neuromuscular junctions. J Biol Chem 268:19152-19159.
122. Rossi SG, Rotundo RL. 1996. Transient interactions between collagen-tailed acetylcholinesterase and sulfated proteoglycans prior to immobilization ion the extracellular matrix. J Biol Chem 271:1979-1987.
123. Rossi SG, Katz S, Rotundo RL. 1998. Control of acetylcholinesterase gene expression in tissue-cultured skeletal muscle: opposite regulation by protein kinases A and C. J Physiol (Paris) 92:486-487.
124. Rotundo RL. 1984. Asymmetric acetylcholinesterase is assembled in the Golgi apparatus. Proc Natl Acad Sci USA 81:479-483.
125. Rotundo RL. 1988. Biogenesis of acetylcholinesterase molecular forms in muscle. Evidence for a rapidly turning over, catalytically inactive precursor pool. J Biol Chem 263:19398-19406.
126. Rotundo RL. 1990. Nucleus-specific translation and assembly of acetylcholinesterase in multinucleated muscle cells. J Cell Biol 110: 715-719.
127. Rotundo RL, Carbonetto ST. 1987. Neurons segregate clusters of membrane-bound acetylcholinesterase along their neurites. Proc Natl Acad Sci USA 84:2063-2067.
128. Rotundo RL, Fambrough DM. 1980a) Secretion of acetylcholinesterase: relation to acetylcholine receptor metabolism. Cell,22:595-602.
129. Rotundo RL, Fambrough DM. 1980b) Synthesis, transport and fate of acetylcholinesterase in cultured chick embryos muscle cells. Cell 22:583-594.
130. Rotundo RL, Gomez AM, Fernandez-Valle C, Randall WR. 1988. Allelic variants of acetylcholinesterase: genetic evidence that all acetylcholinesterase forms in avian nerves and muscles are encoded by a single gene. Proc Natl Acad Sci USA 85:7805-7809.
131. Salpeter MM. 1969. Electron microscope radioautography as a quantitative tool in enzyme cytochemistry. II. The distribution of DFP-reactive sites at motor end-plates of a vertabrate twitch muscle. J Cell Biol 42:122-134.
132. Salpeter MM, Plattner H, Rogers AW. 1972. Quantitative assay of esterases in end-plates of mouse diaphragm by electron micro autoradiography. J Histochem Cytochem 20:1059-1068.
133. Salpeter MM, Rogers AW, Kasprzak H, McHenry FA. 1978. Acetylcholinesterase in the fast extraocular muscle of the mouse by light and electron microscope autoradiography. J Cell Biol 78:274-285.
134. Sanes JR, Lichtman JW. 1999. Development of the vertebrate neuromuscular junction. Annu Rev Neurosci 22:389-442.
135. Saxena A, Ashani Y, Raveh L, Stevenson D, Patel T, Doctor BP. 1998. Role of oligosaccharides in the pharmacokinetics of tissue-derived and genetically engineered cholinesterases. Mol Pharmacol 53:112-122.
136. Schumacher M, Camp S, Maulet Y, Newton M, MacPhee-Quigley K, Taylor SS, Friedmann T, Taylor P. 1986. Primary structure of Torpedo californica acetylcholinesterase deduced from its cDNA sequence. Nature 319:407-409.
137. Scott LJ.C, Bacou F, Sanes JR. 1988. A synapse-specific carbohydrate at the neuromuscular junction: association with both acetylcholinesterase and a glycolipid. J Neurosci 8:932-944.
138. Sikorav JL, Krejci E, Massoulíe J. 1987. cDNA sequences of Torpedo marmorata acetylcholinesterase: primary structure of the precursor of a catalytic subunit; existence of multiple 5'-untranslated regions. EMBO J 6:1865-1873.
139. Simon S, Krejci E, Massoulié J. 1998. 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 17:6178-6187.
140. Sketelj J. 1994. Neural regulation of acetylcholinesterase in skeletal muscles. BAM 4:281-291.
141. Sketelj J, Leisner E, Gohlsch B, Skorjanc D, Pette D. 1997. Specific impulse patterns regulate acetylcholinesterase activity in skeletal muscles of rats and rabbits. J Neurosci Res 47:49-57.
142. Sketelj J, Çrne-Finderle N, Brzin M. 1992b) Influence of denervation on the molecular forms of junctional and extrajunctional acetylcholinesterase in fast and slow muscles of the rat. Neurochem Int 21:415-421.
143. Soreq H, Ben-Aziz R, Prody CA, Seidman S, Gnatt A, Neville L, Lieman-Hurwitz J, Lev-Lehman E, Ginzberg D, Lapidot-Lifson, Y Zakut H. 1990. Molecular cloning and construction of the coding region for human acetylcholinesterase reveals a G+C-rich attenuating structure. Proc Natl Acad Sci USA 87:9688-9692.
144. Stedman E, Easson LH. 1932. Choline-esterase. An enzyme present in the blood serum of the horse. Biochem J 26:2056-2066.
145. Sussman JL, Harel M, Frolow F, Oefner C, Goldman A, Toker L, Silman I. 1991. Atomic structure of acetylcholinesterase from Torpedo californica: a prototypic acetylcholine-binding protein. Science 253:872-879.
146. Talts JF, Andac Z, Gohring W, Brancaccio A, Timpl R. 1999. Binding of the G domains of laminin alpha1 and alpha2 chains and perlecan to heparin, sulfatides, alpha-dystroglycan and several extracellular matrix proteins. EMBO J 18:863-870.
147. Taylor P. 1992. Impact of recombinant DNA technology and protein structure determination on past and future studies on acetylcholinesterase. In: Shafferman A, Velan B, ediotrs. Multidisciplinary approaches to cholinesterase functions. New York: Plenum Press, p 1-15.
148. Taylor PB, Rieger F, Shelanski ML, Greene LA. 1981. Cellular localization of the multiple molecular forms of acetylcholinesterase in cultured neuronal cells. J Biol Chem 256:3827-3830.
149. Toutant JP, Massoulié J. 1988. Cholinesterases: tissue and cellular distribution of molecular forms and their physiological regulation. Handbk Exp Pharmacol 86:225-265.
150. Tsim KW, Randall WE, Barnard EA. 1988. Monoclonal antibodies specific for the different subunits of asymmetric acetylcholinesterase from chick muscle. J Neurochem 51:95-104.
151. Tsim KW, Greenberg I, Rimer M, Randall WR, Salpeter MM. 1992. Transcripts for the acetylcholine receptor and acetylcholine esterase show distribution differences in cultured chick muscle cells. J Cell Biol 118:1201-1212.
152. Tsim KW, Choi RC, Dong TT, Wan DC. 1997. A globular, not asymmetric, form of acetylcholinesterase is expressed in chick motor neurons: down-regulation toward maturity and after denervation. J Neurochem 68:479-487.
153. Valletta FM, Massoulié J. 1991. Regulation of the expression of acetylcholinesterase by muscular activity in avian primary cultures. J Neurochem 56:1518-1525.
154. Velan B, Grosfeld H, Kronman C, Leitner M, Gozes Y, Lazar A, Flashner Y, Marcus D, Cohen S, Shafferman A. 1991. The effect of elimination of intersubunit disulfide bonds on the activity, assembly, and secretion of recombinant human acetylcholinesterase. Expression of acetylcholinesterase Cys-580→Ala mutant. J Biol Chem 266:23977-23984.
155. Velan B, Kronman C, Ordentlich A, Flashner Y, Leitner M, Cohen S, Shafferman A. 1993. N-glycosylation of human acetylcholinesterase: effects on activity, stability and biosynthesis. Biochem J 296:649-656.
156. Velan B, Kronman C, Flashner Y, Shafferman A. 1994. Reversal of signal-mediated cellular retention by subunit assembly of human acetylcholinesterase. J Biol Chem 269:22719-22725.
157. Vellom DC, Radic. Z, Li Y, Pickering NA, Camp S, Taylor P. 1993. Amino acid residues controlling acetylcholinesterase and butyrylcholinesterase specificity. Biochemistry 32:12-17.
158. Vigny M, Gisiger V, Massoulié J. 1978. "Nonspecific" cholinesterase and acetylcholinesterase in rat tissues: molecular forms, structural and catalytic properties, and significance of the two enzyme systems. Proc Natl Acad Sci USA 75:2588-2592.
159. Vigny M, Koenig J, Rieger F. 1976. The motor end-plate specific form of acetylcholinesterase: appearance during embryogenesis and reinnervation of rat muscle. J Neurochem 27:1347-1353.
160. Vigny M, Martin GR, Grotendorst GR. 1983. Interactions of asymmetric forms of acetylcholinesterase with basement membrane components. J Biol Chem 258:8794-8798.
161. Wallace BG, Nitkin RM, Reist NE, Fallon JR, Moayeri NN, McMahan UJ. 1985. Aggregates of acetylcholinesterase induced by acetylcholine receptor-aggregating factor. Nature 315:574-577.
162. Weinberg CB, Hall ZW. 1979. Junctional form of acetylcholinesterase restored at nerve-free endplates. Dev Biol 68:631-635.
163. Weinberg CB, Reiness CG, Hall ZW. 1981. Topographical segregation of old and new acetylcholine receptors at developing ectopic endplates in adult rat muscle. J Cell Biol 88:215-218.
164. Yang X, Fyodorov D, Deneris ES. 1995. Transcriptional analysis of acetylcholine receptor alpha 3 gene promoter motifs that bind Sp1 and AP2. J Biol Chem 270:8514-8520.
165. Younkin SG, Rosenstein C, Collins PL, Rosenberry TL. 1982. Cellular localization of the molecular forms of acetylcholinesterase in rat diaphragm. J Biol Chem 257:13630-13637.
166. Ziskind-Conhaim L, Inestrosa NC, Hall ZW. 1984. Acetylcholinesterase is functional in embryonic rat muscle before its accumulation at the sites of nerve-muscle contact. Dev Biol 103:369-377.