Lithium inhibits a late step in agrin-induced AChR aggregation

Journal of Neurobiology

Volumn 54, Issue 2, 2003, Pages 346-357

  Sharma, S K ^a,b   Wallace, B G ^b  

^a UNIVERSITY OF COLORADO   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Acetylcholine receptor; Agrin; Lithium; Neuromuscular junction; Postsynaptic specializations; Receptor aggregation

Indexed keywords

AGRIN; BETA CATENIN; CHOLINERGIC RECEPTOR; LITHIUM; META TYROSINE; MUSCLE SPECIFIC KINASE; PROTEIN; PROTEIN KINASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; AUTOPHOSPHORYLATION; CAPPING PHENOMENON; CHICK EMBRYO; CONTROLLED STUDY; CYTOSKELETON; EMBRYO; MYOTUBE; NEUROMUSCULAR SYNAPSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

AGRIN; ANIMALS; BENZAZEPINES; BETA CATENIN; BLOTTING, WESTERN; BUNGAROTOXINS; CHICK EMBRYO; CULTURE TECHNIQUES; CYTOSKELETAL PROTEINS; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG INTERACTIONS; ENZYME INHIBITORS; FLUORESCENCE; INDOLES; LITHIUM; MUSCLE FIBERS; NERVE TISSUE PROTEINS; PHOSPHORYLATION; PROTEIN-TYROSINE KINASES; RECEPTOR AGGREGATION; RECEPTOR PROTEIN-TYROSINE KINASES; RECEPTORS, CHOLINERGIC; TIME FACTORS; TRANS-ACTIVATORS;

EID: 0037413907     PISSN: 00223034     EISSN: None     Source Type: Journal    
DOI: 10.1002/neu.10134     Document Type: Article

References (68)

1. Apel ED, Glass DJ, Moscoso LM, Yancopoulos GD, Sanes JR. 1997. Rapsyn is required for MuSK signaling and recruits synaptic components to a MuSK-containing scaffold. Neuron 18:623-635.
2. + in the treatment of bipolar disorder. Trend Neurosci 18:343-349.
3. Axelrod D, Ravdin P, Koppel E, Schlessinger J, Webb WW, Elson EL, Podleski TR. 1976. Lateral motion of fluorescently labeled acetylcholine receptors in membranes of developing muscle fibers. Proc Natl Acad Sci USA 73: 4594-4598.
4. Berzin TM, Zipser BD, Rafii MS, Kuo-Leblanc V, Yancopoulos GD, Glass DJ, Fallon JR, Stopa EG. 2000. Agrin and microvascular damage in Alzheimer's disease. Neurobiol Aging 21:349-355.
5. Borges LS, Ferns M. 2001. Agrin-induced phosphorylation of the acetylcholine receptor regulates cytoskeletal anchoring and clustering. J Cell Biol 153:1-11.
6. Burgess RW, Nguyen QT, Son YJ, Lichtman JW, Sanes JR. 1999. Alternatively spliced isoforms of nerve- and muscle-derived agrin: Their roles at the neuromuscular junction. Neuron 23:33-44.
7. Chapin SJ, Lue CM, Yu MT, Bulinski JC. 1995. Differential expression of alternatively spliced forms of MAP4: a repertoire of structurally different microtubule-binding domains. Biochemistry 34:2289-2301.
8. Coghlan MP, Culbert AA, Cross AE, Cocoran SL, Yates JW, Pearce NJ, Rausch OL, Murphy GJ, Carter PS, Roxbee Cox L, et al. 2000. Selective small molecule inhibitors of glycogen synthase kinase-3 modulate glycogen metabolism and gene transcription. Chem Biol 7:793-803.
9. Connolly JA. 1984. Role of the cytoskeleton in the formation, stabilization, and removal of acetylcholine receptor clusters in cultured muscle cells. J Cell Biol 99:148-154.
10. Dai Z, Luo X, Xie H, Peng HB. 2000. The actin-driven movement and formation of acetylcholine receptor clusters. J Cell Biol 150:1321-1334.
11. Davies SP, Reddy H, Caivano M, Cohen P. 2000. Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem J 351:95-105.
12. 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 85:501-512.
13. Englander LL, Rubin LL. 1987. Acetylcholine receptor clustering and nuclear movement in muscle fibers in culture. J Cell Biol 104:87-95.
14. Falconer MM, Echeverri CJ, Brown DL. 1992. Differential sorting of beta tubulin isotypes into colchicine-stable microtubules during neuronal and muscle differentiation of embryonal carcinoma cells. Cell Mobil Cytoskel 21: 313-325.
15. Ferns M, Deiner M, Hall Z. 1996. Agrin-induced acetylcho-line receptor clustering in mammalian muscle requires tyrosine phosphorylation. J Cell Biol 132:937-944.
16. Fischbach GD. 1972. Synapse formation between dissociated nerve and muscle cells in low density cultures. Dev Biol 28:407-429.
17. Fu AKY, Smith FD, Zhou H, Chu AH, Tsim KWK, Peng BH, Ip NY. 1999. Xenopus muscle-specific kinase: molecular cloning and prominent expression in neural tissues during early embryonic development. Eur J Neurosci 11:373-382.
18. 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.
19. Fuhrer C, Hall ZW. 1996. Functional interaction of src family kinases with the acetylcholine receptor in C2 myotubes. J Biol Chem 271:32474-32481.
20. 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.
21. Gautam M, Noakes PG, Mudd J, Nichol M, Chu GA, Sanes JR, Merlie JP. 1995. Failure of postsynaptic specialization to develop at neuromuscular junctions of rapsyndeficient mice. Nature 377:232-236.
22. Glass DJ, Apel ED, Shah S, Bowen DC, DeChiara TM, Stitt TN, Sanes JR, Yancopoulos GD. 1997. Kinase domain of the muscle-specific receptor tyrosine kinase (MuSK) is sufficient for phosphorylation but not clustering of acetylcholine receptors: Required role for the MuSK ectodomain? Proc Natl Acad Sci USA 94:8848-8853.
23. Glass DJ, Bowen DC, Stitt TN, Radziejewski C, Bruno J, Ryan TE, Gies DR, Shah S, Mattsson K, Burden SJ, DiStefano PS, Valenzuela DM, DeChiara TM, Yancopoulos GD. 1996. Agrin acts via a MuSK receptor complex. Cell 85:513-523.
24. Goold RG, Owen R, Gordon Weeks PR. 1999. Glycogen synthase kinase-3β phosphorylation of MAP-1B regulates the stability of microtubules in growth cones. J Cell Sci 112:3373-3384.
25. Gotz J, Nitsch RM. 2001. Compartmentalized tau hyperphosphorylation and increased levels of kinases in transgenic mice. NeuroReport 12:2007-2016.
26. Gu Y, Oyama F, Ihara Y. 1996. Tau is widely expressed in rat tissues. J Neurochem 67:1235-1244.
27. Hedgepeth CM, Conrad LJ, Zhang J, Huang HC, Lee VM, Klein PS. 1997. Activation of the Wnt signaling pathway: a molecular mechanism for lithium action. Dev Biol 185:82-91.
28. Hong M, Chen DCR, Klein PS, Lee VM-Y. 1997. Lithium reduces tau phosphorylation by inhibition of glycogen synthase kinase-3. J Biol Chem 272:25326-25332.
29. Hopf C, Hoch W. 1997. Heparin inhibits acetylcholine receptor aggregation at two distinct steps in the agrininduced pathway. Eur J Neurosci 9:1170-1177.
30. Hopf C, Hoch W. 1998. Dimerization of the muscle-specific kinase induces tyrosine phosphorylation of acetylcholine receptors and their aggregation on the surface of myotubes. J Biol Chem 273:6467-6473.
31. Jacobson C, Cote PD, Rossi SG, Rotundo RL, Carbonetto S. 2001. The dystroglycan complex is necessary for stabilization of acetylcholine receptor clusters at neuromuscular junctions and formation of the synaptic basement membrane. J Cell Biol 152:435-450.
32. Jasmin BJ, Changeux JP, Cartaud J. 1990. Compartmentalization of cold-stable and acetylated microtubules in the subsynaptic domain of chick skeletal muscle fibre. Nature 344:673-675.
33. Jones MA, Werle MJ. 2000. Nitric oxide is a downstream mediator of agrin-induced acetylcholine receptor aggregation. Mol Cell Neurosci 16:649-660.
34. Klein PS, Melton DA. 1996. A molecular mechanism for the effect of lithium on development. Proc Natl Acad Sci USA 93:8455-8459.
35. Kneussel M, Betz H. 2000. Receptors, gephyrin and gephyrin-associated proteins: novel insights into the assembly of inhibitory postsynaptic membrane specializations. J Physiol (London) 525:1-9.
36. Laemmli UK. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature (London) 227:680-685.
37. Lin W, Burgess RW, Dominguez B, Pfaff SL, Sanes JR, Lee K-F. 2001. Distinct roles of nerve and muscle in postsynaptic differentiation of the neuromuscular synapse. Nature 410:1057-1064.
38. Lucas FR, Goold RG, Gordon-Weeks PR, Salinas PC. 1998. Inhibition of GSK-3beta leading to loss of phosphorylated MAP-1β is an early event in axonal remodeling induced by WNT-7a or lithium. J Cell Sci 111:1351-1361.
39. Lucas FR, Salinas PC. 1997. WNT-7a induces axonal remodeling and increases synapsin I levels in cerebellar neurons. Dev Biol 192:31-44.
40. Mantych KB, Ferreira A. 2001. Agrin differentially regulates the rates of axonal and dendritic elongation in cultured hippocampal neurons. J Neurosci 21:6802-6809.
41. McIntyre RS, Mancini DA, Parikh S, Kennedy SH. 2001. Lithium revisited. Can J Psychiatry 46:322-327.
42. Meier T, Gesemann M, Cavalli V, Ruegg MA, Wallace BG. 1996. AChR phosphorylation and aggregation induced by an agrin fragment that lacks the binding domain for α-dystroglycan. EMBO J 15:2625-2631.
43. Meier T, Perez GM, Wallace BG. 1995. Immobilization of nicotinic acetylcholine receptors in mouse C2 myotubes by agrin-induced protein tyrosine phosphorylation. J Cell Biol 131:441-451.
44. Meyer G, Wallace BG. 1998. Recruitment of a nicotinic acetylcholine receptor mutant lacking cytoplasmic tyrosine residues in its β subunit into agrin-induced aggregates. Mol Cell Neurosci 11:324-333.
45. Mittaud P, Marangi PA, Erb-Vögtli S, Fuhrer C. 2001. Agrin-induced activation of acetylcholine receptor-bound Src family kinases requires rapsyn and correlates with acetylcholine receptor clustering. J Biol Chem 276:14505-14513.
46. Mohamed AS, Rivas-Plata KA, Krass JR, Saleh SM, Swope SL. 2001. Src-class kinases act within the agrin/MuSK pathway to regulate acetylcholine receptor phosphorylation, cytoskeletal anchoring, and clustering. J Neurosci 21:3806-3818.
47. Mohamed AS, Swope SL. 1999. Phosphorylation and cytoskeletal anchoring of the acetylcholine receptor by Src class protein-tyrosine kinases. J Biol Chem 274:20529-20539.
48. Nimnual AS, Chang W, Chang N-S, Ross AF, Gelman MS, Prives JM. 1998. Identification of phosphorylation sites on AChR δ-subunit associated with dispersal of AChR clusters on the surface of muscle cells. Biochemistry 37:14823-14832.
49. Pedrotti B, Islam K. 1996. Dephosphorylated but not phosphorylated microtubule associated protein MAP1B binds to microfilaments. FEBS Lett 388:131-133.
50. Prives J, Fulton AB, Penman S, Daniels MP, Christian CN. 1982. Interaction of the cytoskeletal framework with acetylcholine receptor on the surface of embryonic muscle cells in culture. J Cell Biol 92:231-236.
51. Sanchez C, Perez M, Avila J. 2000. GSK3beta-mediated phosphorylation of the microtubule-associated protein 2C (MAP2C) prevents microtubule bundling. Eur J Cell Biol 79:252-260.
52. Sander A, Hesser BA, Witzemann V. 2001. MuSK induces in vivo acetylcholine receptor clusters in a ligand-independent manner. J Cell Biol 155:1287-1296.
53. Sanes JR, Lichtman JW. 1999. Development of the vertebrate neuromuscular junction. Annu Rev Neurosci 22: 389-442.
54. Sheng M, Lee SH. 2000. Growth of the NMDA receptor industrial complex. Nature Neurosci 3:633-635.
55. Smith CL, Mittaud P, Prescott ED, Fuhrer C, Burden SJ. 2001. Src, Fyn, and Yes are not required for neuromuscular synapse formation but are necessary for stabilization of agrin-induced clusters of acetylcholine receptors. J Neurosci 21:3151-3160.
56. Stambolic V, Ruel L, Woodgett JR. 1996. Lithium inhibits glycogen synthase kinase-3 activity and mimics wingless signaling in intact cells. Curr Biol 6:1664-1668.
57. Takahashi M, Yasutake K, Tomizawa K. 1999. Lithium inhibits neurite growth and tau protein kinase I/ glycogen synthase kinase-3 beta-dependent phosphorylation of juvenile tau in cultured hippocampal neurons. J Neurochem 73:2073-2083.
58. ++ and phorbol ester. J Cell Biol 107:267-278.
59. Wallace BG. 1989. Agrin-induced specializations contain cytoplasmic, membrane and extracellular matrix-associated components of the postsynaptic apparatus. J Neurosci 9:1294-1302.
60. Wallace BG. 1990. Inhibition of agrin-induced acetylcholine-receptor aggregation by heparin, heparan sulfate, and other polyanions. J Neurosci 10:3576-3582.
61. Wallace BG. 1992. Mechanism of agrin-induced acetylcholine receptor aggregation. J Neurobiol 23:592-604.
62. Wallace BG. 1994. Staurosporine inhibits agrin-induced acetylcholine receptor phosphorylation and aggregation. J Cell Biol 125:661-668.
63. Wallace BG. 1995. Regulation of the interaction of nicotinic acetylcholine receptors with the cytoskeleton by agrin-activated protein tyrosine kinase. J Cell Biol 128:1121-1129.
64. Wallace BG, Qu Z, Huganir RL. 1991. Agrin induces phosphorylation of the nicotinic acetylcholine receptor. Neuron 6:869-878.
65. Wells DG, McKechnie BA, Kelkar S, Fallon JR. 1999. Neurotrophins regulate agrin-induced postsynaptic differentiation. Proc Natl Acad Sci USA 96:1112-1117.
66. Weston C, Yee B, Hod E, Prives J. 2000. Agrin-induced acetylcholine receptor clustering is mediated by the small guanosine triphosphatases Rac and Cdc42. J Cell Biol 150:205-212.
67. Williams RSB, Harwood AJ. 2000. Lithium therapy and signal transduction. Trends Pharmacol Sci 21:61-64.
68. Yang X, Arber S, William C, Li L, Tanabe Y, Jessell TM, Birchmeier C, Burden SJ. 2001. Patterning of muscle acetylcholine receptor gene expression in the absence of motor innervation. Neuron 30:399-410.