α-Dystroglycan functions in acetylcholine receptor aggregation but is not a coreceptor for agrin-MuSK signaling

Journal of Neuroscience

Volumn 18, Issue 16, 1998, Pages 6340-6348

  Jacobson, Christian ^a   Montanaro, Federica ^a   Lindenbaum, Michael ^a   Carbonetto, Salvatore ^a   Ferns, Michael ^a,b  

^a MCGILL UNIVERSITY   (Canada)

^b MONTREAL GENERAL HOSPITAL   (Canada)

Author keywords

Acetylcholine receptor; Agrin; Dystroglycan; Neuromuscular junction; Phosphorylation; Synaptogenesis

Indexed keywords

AGRIN; CHOLINERGIC RECEPTOR; DYSTROGLYCAN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; MOUSE; NEUROMUSCULAR SYNAPSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CROSS LINKING; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; SYNAPTOGENESIS;

EID: 0032529544     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.18-16-06340.1998     Document Type: Article

References (29)

1. Apel ED, Roberds SL, Campbell KP, Merlie JP (1995) Rapsyn may function as a link between the acetylcholine receptor and the agrin-binding dystrophin-associated glycoprotein complex. Neuron 15:115-126.
2. 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.
3. Bowe MA, Fallon JR (1995) The role of agrin in synapse formation. Annu Rev Neurosci 18:443-462.
4. Bowe MA, Fallon JR (1996) α-Dystroglycan binds heparin. Soc Neurosci Abstr 22:536.
5. Bowe MA, Deyst KA, Leszyk JD, Fallon JR (1994) Identification and purification of an agrin receptor from Torpedo postsynaptic membranes: a heteromeric complex related to the dystroglycans. Neuron 12:1173-1180.
6. Bowen DC, Sugiyama J, Ferns M, Hall ZW (1996) Neural agrin activates a high-affinity receptor in C2 muscle cells that is unresponsive to muscle agrin. J Neurosci 16:3791-3797.
7. Campanelli JT, Roberds SL, Campbell KP, Scheller RH (1994) A role for dystrophin-associated glycoproteins and utrophin in agrin-induced AChR clustering. Cell 77:663-674.
8. Campanelli JT, Gayer CG, Scheller RH (1996) Alternative RNA splicing that determines agrin activity regulates binding to heparin and alpha-dystroglycan. Development 122:1663-1672.
9. Carbonetto S, Lindenbaum M (1995) The basement membrane at the neuromuscular junction: a synaptic mediatrix. Curr Opin Neurbiol 5:596-605.
10. Chiba A, Matsumura K, Yamada H, Inazu T, Shimizu T, Kusunoki S, Kanazawa I, Kobata A, Endo T (1997) Structures of sialylated O-linked oligosaccharides of bovine peripheral nerve α-dystroglycan. J Biol Chem 272:2156-2162.
11. Cohen MW, Jacobson C, Godfrey EW, Campbell KP, Carbonetto S (1995) Distribution of α-dystroglycan during embryonic nerve-muscle synaptogenesis. J Cell Biol 129:1093-1101.
12. Cohen MW, Jacobson C, Yurchenco PD, Morris GE, Carbonetto S (1997) Laminin-induced clustering of dystroglycan on embryonic muscle cells: comparison with agrin-induced clustering. J Cell Biol 136:1047-1058.
13. DeChiara TM, Bowen DC, Valenzuela DM, Simmons M V, Poueymirou WT, Thomas S, Kinetz E, Compton DL, Rojas E, Park JS, Smith C, DiStefano 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.
14. Ferns M, Hoch W, Campanelli JT, Rupp F, Hall ZW, Scheller RH (1992) RNA splicing regulates agrin-mediated acetylcholine receptor clustering activity on cultured myotubes. Neuron 8:1079-1086.
15. Ferns MJ, Campanelli JT, Hoch W, Scheller RH, Hall Z (1993) The ability of agrin to cluster AChRs depends on alternative splicing and on cell surface proteoglycans. Neuron 11:491-502.
16. Ferns M, Deiner M, Hall Z (1996) Agrin-induced acetylcholine receptor clustering in mammalian muscle requires tyrosine phosphorylation. J Cell Biol 132:937-944.
17. Froehner SC (1991) The submembrane machinery for nicotinic acetylcholine receptor clustering. J Cell Biol 114:1-7.
18. 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.
19. Gee SH, Blacher RW, Douville PJ, Provost PR, Yurchenco PD, Carbonetto S (1993) Laminin-binding protein LBP120 from brain is closely related to the dystrophin-associated glycoprotein dystroglycan and binds with high affinity to the major heparin binding domain of laminin. J Biol Chem 268:14972-14980.
20. Gee SH, Montanaro F, Lindenbaum MH, Carbonetto S (1994) Dystroglycan-a, a dystrophin-associated glycoprotein, is a functional agrin receptor. Cell 77:675-686.
21. Gesemann M, Denzer AJ, Ruegg MA (1995) Acetylcholine receptor aggregating activity of agrin isoforms and mapping of the active site. J Cell Biol 128:625-636.
22. Gesemann M, Cavalli V, Denzer AJ, Brancaccio A, Schumacher B, Ruegg MA (1996) Alternative splicing of agrin alters its binding to heparin, dystroglycan, and the putative agrin receptor. Neuron 16:755-767.
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. 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.
25. Hall ZW, Sanes JR (1993) Synaptic structure and development: the neuromuscular junction. Neuron 10[Suppl]:99-121.
26. Hirano Y, Kidokoro Y (1989) Heparin and heparan sulfate partially inhibit induction of acetylcholine receptor accumulation by nerve in Xenopus culture. J Neurosci 9:1555-1561.
27. Hoch W, Campanelli JT, Harrison S, Scheller RH (1994) Structural domains of agrin required for clustering of nicotinic acetylcholine receptors. EMBO J 13:2814-2821.
28. Hopf C, Hoch W (1996) Agrin binding to alpha-dystroglycan. Domains of agrin necessary to induce acetylcholine receptor clustering are overlapping but not identical to the alpha-dystroglycan-binding region. J Biol Chem 271:5231-5236.
29. Hopf C, Hoch W (1997) Heparin inhibits acetylcholine receptor aggregation at two distinct steps in the agrin-induced pathway. Eur J Neurosci 9:1170-1177.