Rapsyn is required for MuSK signaling and recruits synaptic components to a musk-containing scaffold

Neuron

Volumn 18, Issue 4, 1997, Pages 623-635

  Apel, Elizabeth D ^a   Glass, David J ^b   Moscoso, Lisa M ^a   Yancopoulos, George D ^b   Sanes, Joshua R ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b REGENERON PHARMACEUTICALS INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AGRIN; CHOLINERGIC RECEPTOR; CYTOPLASM PROTEIN; PROTEIN TYROSINE KINASE; RECEPTOR PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; QUAIL; SIGNAL TRANSDUCTION; SYNAPTOGENESIS;

EID: 0030940161     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0896-6273(00)80303-7     Document Type: Article

References (53)

1. Apel, E.D., and Merlie, J.P. (1995a). Assembly of the postsynaptic apparatus. Curr. Opin. Neurobiol. 5, 62-67.
2. Apel, E.D., Roberds, S.L., Campbell, K.P., and Merlie, J.P. (1995b). Rapsyn may function as a link between the acetylcholine receptor and the agrin-binding dystrophin-associated glycoprotein complex. Neuron 15, 115-126.
3. Barrantes, F.J., Neugebauer, D.C., and Zingsheim, H.P. (1980). Peptide extraction by alkaline treatment is accompanied by rearrangement of the membrane-bound acetylcholine receptor from Torpedo marmorata. FEBS Lett. 112, 73-78.
4. Bevan, S., and Steinbach, J.H. (1977). The distribution of alpha-bungarotoxin binding sites on mammalian muscle developing in vivo. J. Physiol. 267, 195-213.
5. Bewick, G.S., Nicholson, L.V.B., Young, C., O'Donnell, E., and Slater, C.R. (1992). Different distributions of dystrophin and related proteins at nerve-muscle junctions. Neuroreport 3, 857-860.
6. Blount, P., and Merlie, J.P. (1988). Native folding of an acetylcholine receptor a subunit expressed in the absence of other receptor subunits. J. Biol. Chem. 263, 1072-1080.
7. Bowe, M.A., and Fallon, J.R. (1995). The role of agrin in synapse formation. Annu. Rev. Neurosci. 18, 443-462.
8. Burden, S.J., DePalma, R.L., and Gottesman, G.S. (1983). Crosslinking of proteins in acetylcholine receptor-rich membranes: association between the β-subunit and the 43 kd subsynaptic protein. Cell 35, 687-692.
9. Chen, C., and Okayama, H. (1987). High-efficiency transformation of mammalian cells by plasmid DNA. Mol. Cell. Biol. 7, 2745-2752.
10. DeChiara, T.M., Bowen, D.C., Valenzuela, D.M., Simmons, M.V., Poueymirou, W.T., Thomas, S., Kinetz, E., Compoton, D.L., Rojas, E., Park, J.S., Smith, C., DiStefano, P.S., Glass, D.J., Burden, S.J., and Yancopoulos, G.D. (1996). The receptor tyrosine kinase MuSK is required for neuromuscular junction formation in vivo. Cell 85, 501-512.
11. Duclert, A., and Changeux, J.P. (1995). Acetylcholine receptor gene expression at the developing neuromuscular junction. Physiol. Rev. 75, 339-368.
12. Feany, M.B., Lee, S., Edwards, R.H., and Buckley, K.M. (1992). The synaptic vesicle protein SV2 is a novel type of transmembrane transporter. Cell 70, 861-867.
13. Ferns, M., Campanelli, J.T., Hoch, W., Scheller, R.H., and Hall, Z.M. (1993). The ability of agrin to cluster AChRs depends on alternative splicing and on cell surface proteoglycans. Neuron 11, 491-502.
14. Ferns, M., Deiner, M., and Hall, Z. (1996). Agrin-induced acetylcholine receptor clustering in mammalian muscle requires tyrosine phosphorylation. J. Cell Biol. 132, 937-944.
15. 125I-labeled α-bungarotoxin binding at mouse motor endplates. Proc. Natl. Acad. Sci. USA 71, 1376-1378.
16. r 43,000 protein of Torpedo postsynaptic membrane. Proc. Natl. Acad. Sci. USA 78, 5230-5234
17. Froehner, S.C., Luetje, C.W., Scotland, P.B., and Patrick, J. (1990). The postsynaptic 43K protein clusters muscle nicotinic acetylcholine receptors in Xenopus oocytes. Neuron 5, 403-410.
18. Fuhrer, C., and Hall, Z.W. (1996). Functional interaction of src family kinases with the acetylcholine receptor in C2 myotubes. J. Biol. Chem. 271, 32474-32481.
19. Gautam, M., Noakes, P.G., Mudd, J., Nichol, M. Chu, G.G., Sanes, J.R., and Merlie, J.P. (1995). Failure of postsynaptic specialization to develop at neuromuscular junctions of rapsyn-deficient mice. Nature 377, 232-236.
20. Gautam, M., Noakes, P.G., Moscoso, L.M., Rupp, F., Scheller, R.H., Merlie, J.P.,and Sanes, J.R. (1996). Defective neuromuscular synaptogenesis in agrin-deficient mice. Cell 85, 525-536.
21. Gillespie, S.K.H., Balasubramanian, S., Fung, E.T., and Huganir, R.L. (1996). Rapsyn clusters and activates the synapse-specific receptor tyrosine kinase MuSK. Neuron 16, 953-962.
22. Glass, D.J., Bowen, D.C., Stitt, T.N., Radziejewski, C., Bruno, J., Ryan, T.E., Gies, D.R., Shah, S., Mattsson, K., Burden, S.J., DiStefano, P.S., Valenzuela, D.M., DiChiara, T.M., and Yancopoulos, G.D. (1996). Agrin acts via a MuSK receptor complex. Cell 85, 513-523.
23. Hall, Z.W., and Sanes, J.R. (1993). Synaptic structure and development: The neuromuscular junction. Cell/Neuron 72, 99-121.
24. Henry, M.D., and Campbell, K.P.(1996).Dystroglycan: an extracellular matrix receptor linked to the cytoskeleton. Curr. Opin. Cell Biol. 8, 625-631.
25. Ibraghimov, B.O., Ervasti, J.M., Leveille, C.J., Slaughter, C.A., Sernett, S.W., and Campbell, K.P. (1992). Primary structure of dystrophin-associated glycoproteins linking dystrophin to the extracellular matrix. Nature 355, 696-702.
26. Jennings, C.G.B., Dyer, S.M., and Burden, S.J. (1993). Muscle-specific trk-related receptor with a kringle domain defines a distinct class of receptor tyrosine kinases. Proc. Natl. Acad. Sci. USA 90, 2895-2899.
27. Khurana, T.S., Watkins, S.C., Chafey, P., Chelly, J., Tome, F.M.S., Fardeau, M., Kaplan, J.C., and Kunkel, L.M. (1991). Immunolocalization and developmental expression of dystrophin related protein in skeletal muscle. Neuromusc. Dis. 1, 185-194.
28. LaRochelle, W.J., and Froehner, S.C. (1987). Comparison of the postsynaptic 43-kDa protein from muscle cells that differ in acetylcholine receptor clustering activity. J. Biol. Chem. 262, 8190-8195.
29. Maimone, M.M., and Merlie, J.P. (1993). Interaction of the 43 kd postsynaptic protein with all subunits of the muscle nicotinic acetylcholine receptor. Neuron 11, 53-66.
30. Martinou, J.C., Falls, D.L., Fischbach, G.D., and Merlie, J.P. (1991). Acetylcholine receptor-inducing activity stimulates expression of the ∈-subunit gene of the muscle acetylcholine receptor. Proc. Natl. Acad. Sci. USA 88, 7669-7673.
31. McMahan, U.J. (1990). The agrin hypothesis. Cold Spring Harbor Symp. Quant. Biol. 55, 407-418.
32. Merlie, J.P., and Sanes, J.R. (1985). Concentration of acetylcholine receptor mRNA in synaptic regions of adult muscle fibres. Nature 317, 66-68.
33. Moscoso, L.M., Merlie, J.P., and Sanes, J.R. (1995a). N-CAM, 43K-rapsyn, and s-laminin mRNAs are concentrated at synaptic sites in muscle fibers. Mol. Cell. Neurosci. 6, 80-89.
34. Moscoso, L.M., Chu, G.C., Gautam, M., Noakes, P.G., Merlie, J.P., and Sanes, J.R. (1995b). Synapse-associated expression of an acetylcholine receptor-inducing protein, ARIA/Heregulin, and its putative receptors, erbB2 and erbB3, in developing mammalian muscle. Dev. Biol. 172, 158-169.
35. Moscovici, D., Moscovici, M.G., Jimenez, H., Lai, M.M.C., Hayman, M.J., and Vogt, P.K. (1977). Continuous tissue culture cell lines derived from chemically induced tumors of Japanese quail. Cell 11, 95-103.
36. Noakes, P.G., Phillips, W.D., Hanley, T.A., Sanes, J.R., and Merlie, J.P. (1993). 43k protein and acetylcholine receptors colocalize during the initial stages of neuromuscular synapse formation in vivo. Dev. Biol. 155, 275-280.
37. Ohlendieck, K., Ervasti, J.M., Matsumura, K., Kahl, S.D., Leveille, C.J., and Campbell, K.P. (1991). Dystrophin-related protein is localized to neuromuscular junctions of adult skeletal muscle. Neuron 7, 499-508.
38. Peng, H.B., and Froehner, S.C. (1985). Association of the postsynaptic 43K protein with newly formed acetylcholine receptor clusters in cultured muscle cells. J. Cell Biol. 100, 1698-1705.
39. Peng, H.B., Baker, L.P., and Chen, Q. (1991). Induction of synaptic development in cultured muscle cells by basic fibroblast growth factor. Neuron 6, 237-246.
40. Phillips, W.D., Kopta, C., Blount, P., Gardner, P.D., Steinbach, J.H., and Merlie, J.P. (1991a). ACh receptor-rich membrane domains organized in fibroblasts by recombinant 43-kilodalton protein. Science 251, 568-570.
41. Phillips, W.D., Maimone, M.M., and Merlie, J.P. (1991b).Mutagenesis of the 43-kD postsynaptic protein defines domains involved in plasma membrane targeting and AChR clustering. J. Cell Biol. 115, 1713-1723.
42. Phillips, W.D., Noakes, P.G., Roberds, S.L., Campbell, K.P., and Merlie, J.P. (1993). Clustering and immobilization of acetylcholine receptors by the 43-kD protein: a possible role for dystrophin-related protein. J. Cell Biol. 123, 729-740.
43. Qu, Z., Apel, E.D., Doherty, C.A., Hoffman, P.W., Merlie, J.P., and Huganir, R.L. (1996). The synapse-associated protein rapsyn regulates tyrosine phosphorylation of proteins colocalized at nicotinic acetylcholine receptor clusters. Mol. Cell. Neurosci. 8, 171-184.
44. Riedel, H., Dull, T.J., Honegger, A.M., Schlessinger, J., and Ullrich, A. (1989). Cytoplasmic domains determine signal specificity, cellular routing characteristics and influence ligand binding of epidermal growth factor and insulin receptors. EMBO J. 8, 2943-2954.
45. Rousselet, A., Cartaud, J., Deveaux, P.F., and Changeux, J.-P. (1982). The rotational diffusion of the acetylcholine receptor in Torpedo marmorata membrane fragments studied with a spin-labelled α-toxin: importance of the 43,000 protein(s). EMBO J. 1, 439-445.
46. Sanes, J. (1997). Genetic analysis of postsynaptic differentiation at the vertebrate neuromuscular junction. Curr. Opin. Neurobiol. 7, 93-100.
47. Sanes, J.R., Johnson, Y.R., Kotzbauer, P.T., Mudd, J., Hanley, T., Matinou, J.C., and Merlie, J.P. (1991). Selective expression of an acetylcholine receptor-lacZ transgene in synaptic nuclei of adult muscle fibers. Development 113, 1181-1191.
48. Sealock, R., Barnaby, E.W., and Froehner, S.C. (1984). Ultrastructural localization of the Mr 43,000 protein and the acetylcholine receptor in Torpedo postsynaptic membranes using monoclonal antibodies. J. Cell Biol. 98, 2239-2244.
49. Tzartos, S.J., Rand, D.E., Einarson, B.L., and Lindstrom, J.M. (1981). Mapping of surface structures of electrophorus acetylcholine receptors using monoclonal antibodies. J. Biol. Chem. 256, 8635-8645.
50. Tzartos, S., Langeberg, L., Hochschwender, S., Swanson, L.W., and Lindstrom, J. (1986). Characteristics of monoclonal antibodies to denatured Torpedo and to native calf acetylcholine receptors: species, subunit, and region specificity. J. Neuroimmunol. 10, 235-253.
51. Valenzuela, D.M., Stitt, T.N., DiStefano, P.S., Rojas, E., Mattsson, K., Compton, D.L., Nunez, L., Park, J.S., Stark, J.L., Geis, D.R., Thomas, S., LeBeau, M.M., Fernald, A.A., Copeland, N.G., Jenkins, N.A., Burden, S.J., Glass, D.J., and Yancopoulos, G.D. (1995). Receptor tyrosine kinase specific for the skeletal muscle lineage: expression in embyronic muscle, at the neuromuscular junction, and after injury. Neuron 15, 573-584.
52. Wallace, B.G. (1994). Staurosporine inhibits agrin-induced acetylcholine receptor phosphorylation and aggregation. J. Cell Biol. 125, 661-668.
53. Wallace, B.G., Qu, Z., and Huganir, R.L. (1991). Agrin induces phosphorylation of the nicotinic acetylcholine receptor. Neuron 6, 869-878.