ATP acts via P2Y1 receptors to stimulate acetylcholinesterase and acetylcholine receptor expression: Transduction and transcription control

Journal of Neuroscience

Volumn 23, Issue 11, 2003, Pages 4445-4456

  Choi, Roy C Y ^a   Siow, Nina L ^a   Cheng, Anthony W M ^a   Ling, Karen K Y ^a   Tung, Edmund K K ^a   Simon, Joseph ^b   Barnard, Eric A ^b   Tsim, Karl W K ^a  

^a HONG KONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Hong Kong)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Acetylcholine receptor; Acetylcholinesterase; ATP receptors; Elk 1; Gene regulation; Neuromuscular junction; P2Y1 receptor; Trophic factors

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; ACETYLCHOLINESTERASE; ADENOSINE TRIPHOSPHATE; CALCIUM ION; CHOLINERGIC RECEPTOR; COMPLEMENTARY DNA; DANTROLENE; ETHYLENE GLYCOL 1,2 BIS(2 AMINOPHENYL) ETHER N,N,N',N' TETRAACETIC ACID; PHORBOL 13 ACETATE 12 MYRISTATE; PROTEIN KINASE C; PURINE P2Y RECEPTOR; RECEPTOR SUBTYPE; THAPSIGARGIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR ELK 1; UNCLASSIFIED DRUG; UO 126; VERAPAMIL;

ANIMAL CELL; ARTICLE; CHICK EMBRYO; CONTROLLED STUDY; EMBRYO; GENE ACTIVATION; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETIC TRANSFECTION; IMMUNOBLOTTING; IMMUNOCYTOCHEMISTRY; MYOTUBE; NERVOUS SYSTEM DEVELOPMENT; NEUROMUSCULAR SYNAPSE; NONHUMAN; NORTHERN BLOTTING; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN PHOSPHORYLATION; REPORTER GENE; SIGNAL TRANSDUCTION; SITE DIRECTED MUTAGENESIS; TRANSCRIPTION REGULATION;

EID: 0038795202     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.23-11-04445.2003     Document Type: Article

References (58)

1. Altiok N, Changeux J-P (2001) Electrical activity regulates AChR gene expression via JNK, PKC, and Sp1 in skeletal chick muscle. FEBS Lett 487:333-338.
2. Altiok N, Altiok S, Changeux J-P (1997) Heregulin-stimulated acetylcholine receptor gene expression in muscle: requirement for MAP kinase and evidence for a parallel inhibitory pathway independent of electrical activity. EMBO J 16:717-725.
3. Angus LM, Chan RYY, Jasmin BJ (2001) Role of intronic E- and N-box motifs in the transcriptional induction of the acetylcholinesterase gene during myogenic differentiation. J Biol Chem 276:17603-17609.
4. Ben Aziz-Aloya R, Seidman S, Timberg R, Sternfeld M, Zakut H, Soreq H (1993) Expression of a human acetylcholinesterase promoter-reporter construct in developing neuromuscular junctions of Xenopus embryos. Proc Natl Acad Sci USA 90:2471-2475.
5. 1 receptor. Mol Pharmacol 50:1323-1329.
6. Briguet A, Ruegg MA (2000) The Ets transcription factor GABP is required for postsynaptic differentiation in vivo. J Neurosci 20:5989-5996.
7. Chahine KG, Walke W, Goldman D (1992) A 102 base pair sequence of the nicotinic acetylcholine receptor δ-subunit gene confers regulation by muscle electrical activity. Development 115:213-219.
8. Chan RYY, Boudreau-Lariviere 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.
9. Choi RCY, Yung LY, Dong TTX, Wan DCC, Wong YH, Tsim KWK (1998) The calcitonin gene-related peptide-induced acetylcholinesterase synthesis in cultured chick myotubes is mediated by cyclic AMP. J Neurochem 71:152-160.
10. 1 nucleotide receptor in chick muscle: its functional role in the regulation of acetylcholinesterase and acetylcholine receptor. J Neurosci 21:9224-9234.
11. Choi RCY, Siow NL, Zhu SQ, Wan DCC, Wong YH, Tsim KWK (2001b) The cyclic AMP-mediated expression of acetylcholinesterase in myotubes shows contrasting activation and repression between avian and mammalian enzymes. Mol Cell Neurosci 17:732-745.
12. Cohen I, Rimer M, Lomo T, McMahan UJ (1997) Agrin-induced postsynaptic-like apparatus in skeletal muscle fibers in vivo. Mol Cell Neurosci 9:237-253.
13. Cullen PJ, Lockyer PJ (2002) Integration of calcium and Ras signaling. Nat Rev Mol Cell Biol 3:339-348.
14. Dempsey EC, Newton AC, Mochly-Rosen D, Fields AP, Reyland ME, Insel PA, Messing RO (2000) Protein kinase C isozymes and the regulation of diverse cell responses. Am J Physiol Lung Cell Mol Physiol 279:L429-L438.
15. 7 receptors are targeted to presynaptic terminals in the central and peripheral nervous systems. J Neurosci 21:7143-7152.
16. Duclert A, Changeux J-P (1995) Acetylcholine receptor gene expression at the developing neuromuscular junction. Physiol Rev 75:339-368.
17. Dudley DT, Pang L, Decker SJ, Bridges AJ, Saltiel AR (1995) A synthetic inhibitor of the mitogen-activated protein kinase cascade. Proc Natl Acad Sci USA 92:7686-7689.
18. Favata MF, Horiuchi KY, Manos EJ, Daulerio AJ, Stradley DA, Feeser WS, Van Dyk DE, Pitts WJ, Earl RA, Hobbs F, Copeland RA, Magolda RL, Scherle PA, Trzaskos JM (1998) Identification of a novel inhibitor of mitogen-activated protein kinase kinase. J Biol Chem 273:18623-18632.
19. Fischbach GD, Rosen KM (1997) ARIA: a neuromuscular junction neuregulin. Annu Rev Neurosci 20:429-458.
20. Fuhrer C, Gautam M, Sugiyama JE, Hall ZW (1999) Roles of rapsyn and agrin in interaction of postsynaptic proteins with acetylcholine receptors. J Neurosci 19:6405-6416.
21. Glantz SA (1988) Primer of biostatistics. New York: McGraw-Hill.
22. Grisaru D, Sternfeld M, Eldor A, Glick D, Soreq H (1999) Structural roles of acetylcholinesterase variants in biology and pathology. Eur J Biochem 264:672-686.
23. Hilgenberg L, Yearwood S, Milstein S, Miles K (1996) Neural influence on protein kinase C isoform expression in skeletal muscle. J Neurosci 16:4994-5003.
24. Hodge C, Liao J, Stofega M, Guan K, Carter-Su C, Schwartz J (1998) Growth hormone stimulates phosphorylation and activation of Elk-1 and expression of c-fos, egr-1, and junB through activation of extracellular signal-regulated kinases 1 and 2. J Biol Chem 273:31327-31336.
25. Israel M, Dunant Y (1998) Acetylcholine release and the cholinergic genomic locus. Mol Neurobiol 16:1-20.
26. Jo YH, Schlichter R (1999) Synaptic co-release of ATP and GABA in cultured spinal neurons. Nat Neurosci 2:241-245.
27. Johnson LN, Noble ME, Owen DJ (1996) Active and inactive protein kinases: structural basis for regulation. Cell 85:149-158.
28. 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.
29. Lanuza MA, Li MX, Jia M, Kim S, Davenport R, Dunlap V, Nelson PG (2000) Protein kinase C-mediated changes in synaptic efficacy at the neuromuscular junction in vitro: the role of postsynaptic acetylcholine receptors. J Neurosci Res 61:616-625.
30. Laufer R, Klarsfeld A, Changeux J-P (1991) Phorbol esters inhibit the activity of the chicken acetylcholine receptor α-subunit gene promoter. Role of myogenic regulators. Eur J Biochem 202:813-818.
31. Legay C, Mankal FA, Massoulié J, Jasmin BJ (1999) Stability and secretion of acetylcholinesterase forms in skeletal muscle cells. J Neurosci 19:8252-8259.
32. Li Y, Camp S, Rachinsky TL, Bongiorno C, Taylor P (1993) Promoter elements and transcriptional control of the mouse acetylcholinesterase gene. J Biol Chem 268:3563-3572.
33. Lin W, Burgess RW, Dominguez B, Pfaff SL, Sanes JR, Lee KF (2001) Distinct roles of nerve and muscle in postsynaptic differentiation of the neuromuscular synapse. Nature 410:1057-1064.
34. Macleod K, Leprince D, Stehelin D (1992) The Ets family. Trends Biochem Sci 17:251-256.
35. Macpherson P, Kostrominova T, Tang H, Goldman D (2002) Protein kinase C and calcium/calmodulin-activated protein kinase II (CaMKII) suppress nicotinic acetylcholine receptor gene expression in mammalian muscle. J Biol Chem 277:15638-15646.
36. Massoulié J, Pezzementi L, Bon S, Krejci E, Vallette F-M (1993) Molecular and cellular biology of cholinesterases. Prog Neurobiol 41:31-91.
37. Mineo C, Anderson RG, White MA (1997) Physical association with Ras enhances activation of membrane-bound Raf (RafCAAX). J Biol Chem 272:10345-10348.
38. Mischak H, Seitz T, Janosch P, Eulitz M, Steen H, Schellerer M, Philipp A, Kolch W (1996) Negative regulation of Raf-1 by phosphorylation of serine 621. Mol Cell Biol 16:5409-5418.
39. 1 purinergic receptor: striking neuronal localisation. J Comp Neurol 421:374-384.
40. Murphy LO, Smith S, Chen RH, Fingar DC, Blenis J (2002) Molecular interpretation of ERK signal duration by immediate early gene products. Nat Cell Biol 4:556-564.
41. Perkins GA, Wang L, Huang LJ, Humphries K, Yao VJ, Martone M, Deerinck TJ, Barraclough DM, Violin JD, Smith D, Newton A, Scott JD, Taylor SS, Ellisman MH (2001) PKA, PKC, and AKAP localization in and around the neuromuscular junction. BMC Neurosci 2:17-35.
42. Pun S, Tsim KWK (1995) Truncated form of pro-acetylcholine receptor-inducing activity (ARIA) induces AChR α-subunit but not AChE transcripts in cultured chick myotubes. Neurosci Lett 198:107-110.
43. Pun S, Tsim KWK (1997) Antisense agrin cDNA transfection blocks neuroblastoma cell-induced acetylcholine receptor aggregation when co-cultured with myotubes. Mol Cell Neurosci 10:87-99.
44. Rossi SG, Vazquez AE, Rotundo RL (2000) Local control of acetylcholinesterase gene expression in multinucleated skeletal muscle fibers: individual nuclei respond to signals from the overlying plasma membrane. J Neurosci 20:919-928.
45. Rotundo RL (1988) Biogenesis of acetylcholinesterase molecular forms in muscle. J Biol Chem 263:19398-19406.
46. Sambrook J, Russel DW (2001) Molecular cloning: a laboratory manual, 3rd Ed. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
47. Sanes JR, Lichtman JW (1999) Development of the vertebrate neuromuscular junction. Annu Rev Neurosci 22:389-442.
48. Sanes JR, Johnson YR, Kotzbauer PT, Mudd J, Hanley T, Martinou JC, Merlie JP (1991) Selective expression of an acetylcholine receptor-1acZ transgene in synaptic nuclei of adult muscle fibers. Development 113:1181-1191.
49. Schaeffer L, de Kerchove d'Exaerde A, Changeux J-P (2001) Targeting transcription to the neuromuscular synapse. Neuron 31:15-22.
50. 1 receptor stimulate mitogen-activated protein kinases and induce apoptosis. J Biol Chem 276:16379-16390.
51. Si J, Mei L (1999) ERK MAP kinase activation is required for ARIA-induced increase in all five AChR subunit mRNAs as well as synapse-specific expression of the AChR ε-transgene. Mol Brain Res 67:18-27.
52. Si J, Wang Q, Mei L (1999) Essential roles of c-JUN and c-JUN N-terminal kinase (JNK) in neuregulin-increased expression of the acetylcholine receptor ε-subunit. J Neurosci 19:8498-8508.
53. Silinsky EM, Redman RS (1996) Synchronous release of ATP and neurotransmitter within milliseconds of a motor nerve impulse in the frog. J Physiol (Lond) 492:815-822.
54. Siow NL, Choi RCY, Cheng AWM, Jiang JXS, Wan DCC, Zhu SQ, Tsim KWK (2002) A cyclic AMP-dependent pathway regulates the expression of acetylcholinesterase during myogenic differentiation of C2C12 cells. J Biol Chem 277:36129-36136.
55. Tsim KWK, Barnard EA (2002) The signaling pathways mediated by P2Y nucleotide receptors in the formation and maintenance of the skeletal neuromuscular junction. Neurosignals 11:58-64.
56. Tsim KWK, Randall WR, Barnard EA (1988) Monoclonal antibodies specific for the different subunits of asymmetric acetylcholinesterase from chick muscle. J Neurochem 51:95-104.
57. Walke W, Staple J, Adams L, Gnegy M, Chahine K, Goldman D (1994) Calcium-dependent regulation of rat and chick muscle nicotinic acetylcholine receptor (nAChR) gene expression. J Biol Chem 269:19447-19456.
58. Webb TE, Simon J, Krishek BJ, Bateson AN, Smart TG, King BF, Burnstock G, Barnard EA (1993) Cloning and functional expression of a brain G-protein-coupled ATP receptor. FEBS Lett 324:219-225.