The receptor tyrosine kinase MuSK is required for neuromuscular junction formation in vivo

Cell

Volumn 85, Issue 4, 1996, Pages 501-512

  DeChiara, Thomas M ^a   Bowen, David C ^a   Valenzuela, David M ^a   Simmons, Mary V ^a   Poueymirou, William T ^a   Thomas, Susan ^b   Kinetz, Erika ^b   Compton, Debra L ^a   Rojas, Eduardo ^a   Park, John S ^a   Smith, Cynthia ^b   DiStefano, Peter S ^a   Glass, David J ^a   Burden, Steven J ^b   Yancopoulos, George D ^a  

^a REGENERON PHARMACEUTICALS INC   (United States)

^b NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AGRIN; PROTEIN TYROSINE KINASE;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; EMBRYO; GENE DISRUPTION; GENETIC RECOMBINATION; MOUSE; NERVE CELL DIFFERENTIATION; NEUROMUSCULAR SYNAPSE; NONHUMAN; PRESYNAPTIC NERVE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SYNAPTOGENESIS;

EID: 15844417385     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0092-8674(00)81251-9     Document Type: Article

References (67)

1. Altiok, N., Bessereau, J.L., and Changeux, J.P. (1995). ErbB3 and ErbB2/neu mediate the effect of heregulin on acetylcholine receptor gene expression in muscle: differential expression at the end plate. EMBO J. 14, 4258-4266.
2. Apel, E.D., Roberds, S.L., Campbell, K.P., and Merlie, J.P. (1995). Rapsyn may function as a link between the acetylcholine receptor and the agrin-binding dystrophin-associated glycoprotein complex. Neuron 15, 115-126.
3. Balice-Gordon, R.J., and Lichtman, J.W. (1994). Long-term synapse loss induced by focal blockade of postsynaptic receptors. Nature 372, 519-524.
4. Barbacid, M. (1993). Nerve growth factor: a tale of two receptors. Oncogene 8, 2033-2042.
5. Bowe, M.A., and Fallon, J.R. (1995). The role of agrin in synapse formation. Annu. Rev. Neurosci. 18, 443-462.
6. Bowe, M.A., Deyst, K.A., Leszyk, J.D., and Fallon, J.R. (1994). Identification and purification of an agrin receptor from Torpedo postsynaptic membranes: a heteromeric complex related to dystroglycans. Neuron 12, 1173-1180.
7. Brown, M.C., Holland, R.L., and Hopkins, W.G. (1981). Motor nerve sprouting. Annu. Rev. Neurosci. 4, 17-42.
8. Buckley, K., and Kelly, R.B. (1985). Identification of a transmembrane glycoprotein specific for secretory vesicles of neural and endocrine cells. J. Cell Biol. 100, 1284-1294.
9. Burden, S.J., Sargent, P.B., and McMahan, U.J. (1979). Acetylcholine receptors in regenerating muscle accumulate at original synaptic sites in the absence of the nerve. J. Cell Biol. 82, 412-425.
10. Burden, S.J., Jo, S.A., Tang, J., Zhu, X., Yeadon, J.E., and Simon, A.M. (1995). Polarity in skeletal muscle cells is induced by innervation. Sem. Dev. Biol. 6, 59-65.
11. Campanelli, J.T., Roberds, S.L., Campbell, K.P., and Scheller, R.H. (1994). A role for dystrophin-associated glycoproteins and utrophin in agrin-induced AChR clustering. Cell 77, 663-674.
12. Carraway, K.L., and Burden, S.J. (1995). Neuregulins and their receptors. Curr. Opin. Neurobiol. 5, 606-612.
13. Cartaud, J., and Changeux, J.P. (1993). Post-transcriptional compartmentalization of acetylcholine receptor biosynthesis in the subneural domain of muscle and electrocytejunctions. Eur. J. Neurosci. 5, 191-202.
14. Chu, G.C., Moscoso, L.M., Sliwkowski, M.X., and Merlie, J.P. (1995). Regulation of the acetylcholine receptor ∈ subunit gene by recombinant ARIA: an in vitro model for transynaptic gene regulation. Neuron 14, 329-339.
15. Conover, J.C., Erickson, J.T., Katz, D.M., Bianchi, L.M., Poueymirou, W.T., McClain, J., Pan, L., Helgren, M., Ip, N.Y., Boland, P., Friedman, B., Weigand, S., Vejsada, R., Kato, A., DeChiara, T.M., and Yancopoulos, G.D. (1995). Mice lacking NT4 thrive and retain motoneurones, but exhibit sensory neuron deficits distinct from mice lacking BDNF. Nature 375, 235-238.
16. DeChiara, T.M., Vejsada, R., Poueymirou, W.T., Acheson, A., Suri, C., Conover, J.C., Friedman, B., McClain, J., Pan, L., Stahl, N., Ip, N.Y., Kato, A., and Yancopoulos, G.D. (1995). Mice lacking the CNTF receptor, unlike mice lacking CNTF, exhibit profound motor neuron deficits at birth. Cell 83, 313-322.
17. Duclert, A., and Changeux, J.P. (1995). Acetylcholine receptor gene expression at the developing neuromuscular junction. Physiol. Rev. 75, 339-368.
18. Falls, D.L., Harris, D.A., Johnson, F.A., Morgan, M.M., Corfas, G., and Fischbach, G.D. (1990). Mr 42,000 ARIA: a protein that may regulate the accumulation of acetylcholine receptors at developing chick neuromuscular junctions. Cold Spring Harbor Symp. Quant. Biol. 55, 397-406.
19. Falls, D.L., Rosen, K.M., Corfas, G., Lane, W.S., and Fischbach, G.D. (1993). ARIA, a protein that stimulates acetylcholine receptor synthesis, is a member of the neu ligand family. Cell 72, 801-815.
20. Ferns, M., Camapnelli, J.T., Hoch, W., Scheller, R.H., and Hall, Z.W. (1993). The ability of agrin to cluster AChRs depends on alternative splicing and on cell surface proteoglycans. Neuron 11, 491-502.
21. 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.
22. Fong, G.H., Rossant, J., Gertenstein, M., and Breitman, M.L. (1995). Role of the Flt-1 receptor tyrosine kinase in regulating assembly of vascular endothelium. Nature 376, 66-70.
23. Ganju, P., Walls, E., Brennan, J., and Reith, A.D. (1995). Cloning and developmental expression of NsK2, a novel receptor tyrosine kinase implicated in skeletal myogenesis. Oncogene 11, 281-290.
24. Gautam, M., Noakes, P.G., Mudd, J., Nichol, M., Chu, G.C., 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.
25. Gautam, M., Noakes, P.G., Moscoso, L., Rupp, F., Scheller, R.H., Merlie, J.P., and Sanes, J.R. (1996). Defective neuromuscular synaptogenesis in agrin-deficient mice. Cell, this issue.
26. Gee, S.H., Montanaro, F., Lindenbaum, M.H., and Carbonetto, S. (1994). Dystroglycan-α, a dystrophin-associated glycoprotein, is a functional agrin receptor. Cell 77, 675-686.
27. Glass, D.J., and Yancopoulos, G.D. (1993). The neurotrophins and their receptors. Trends Cell Biol. 3, 262-268.
28. Glass, D.J., Bowen, D.C., Stitt, T.N., Radziejewski, C., Bruno, J., Ryan, T.E., Gies, D.R., Shah, S., Burden, S.J., DiStefano, P.S., Valenzuela, D.M., DeChiara, T.M., and Yancopoulos, G.D. (1996). Agrin acts via a MuSK receptor complex. Cell, this issue.
29. Godfrey, E.W., Nitkin, R.M., Wallace, B.G., Rubin, L.L., and McMahan, U.J. (1984). Components of Torpedo electric organ and muscle that cause aggregation of acetylcholine receptors on cultured muscle cells. J. Cell Biol. 99, 615-627.
30. Goodearl, A.D., Yee, A.G., Sandrock, A.W., Corfas, G., and Fischbach, G.D. (1995). ARIA is concentrated in the synaptic basal lamina of the developing chick neuromuscular junction. J. Cell Biol. 130, 1423-1434.
31. Hall, Z.W., and Sanes, J.R. (1993). Synaptic structure and development: the neuromuscular junction. Cell 72/Neuron 10 (Suppl.), 99-121.
32. Harris, D.A., Falls, D.L., and Fischbach, G.D. (1989). Differential activation of myotube nuclei following exposure to an acetylcholine receptor-inducing factor. Nature 337, 173-176.
33. Helgren, M.E., Squinto, S.P., Davis, H.L., Parry, D.J., Boulton, T.G., Heck, C.S., Zhu, Y., Yancopoulos, G.D., Lindsay, R.M., and DiStefano, P.S. (1994). Trophic effects of ciliary neurotrophic factor on denervated skeletal muscle. Cell 76, 493-504.
34. Hoch, W., Ferns, M., Campanelli, J.T., Hall, Z.W., and Scheller, R.H. (1993). Developmental regulation of highly active alternatively spliced forms of agrin. Neuron 11, 479-490.
35. Jennings, C.G., Dyer, S.M., and Burden, S.J. (1993). Muscle-specific trk-related receptor with a kringle domain defines a distinct class of receptor tyrosinekinases. Proc. Natl. Acad. Sci. USA90, 2895-2899.
36. Jessell, T.M., Siegel, R.E., and Fischbach, G.D. (1979). Induction of acetylcholine receptors on cultured skeletal muscle by a factor extracted from brain and spinal cord. Proc. Natl. Acad. Sci. USA 76, 5397-5401.
37. Jo, S.A., Zhu, X., Marchionni, M .A., and Burden, S.J. (1995). Neuregulins are concentrated at nerve-muscle synapses and activate ACh-receptor gene expression. Nature 373, 158-161.
38. Karnovsky, M.J. (1964). J. Cell Biol. 23, 217-232.
39. Kuffler, D.P. (1986). Accurate reinnervation of motor end plates after disruption of sheath cells and muscle fibers. J. Comp. Neurol. 250, 228-235.
40. Letinsky, M.S., Fischbeck, K.H., and McMahan, U.J. (1976). Precision of reinnervation of original postsynaptic sites in frog muscle after a nerve crush. J. Neurocytol. 5, 691-718.
41. 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 acetylchoine receptor. Proc. Natl. Acad. Sci. USA 88, 7669-7673.
42. Masiakowski, P., and Carroll, R.D. (1992). A novel family of cell surface receptors with tyrosine kinase-like domain. J. Biol. Chem. 267, 26181-26190.
43. McMahan, U.J. (1990). The agrin hypothesis. Cold Spring Harbor Symp. Quant. Biol. 55, 407-418.
44. McMahan, U.J., and Slater, C.R. (1984). The influence of basal lamina on the accumulation of acetylcholine receptors at synaptic sites in regenerating muscles. J. Cell Biol. 98, 1453-1473.
45. Moscoso, L.M., Chu, G.C., Gautam, M., Noakes, P.G., Merlie, J.P., and Sanes, J.R. (1995). 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.
46. Nitkin, R.M., Smith, M.A., Magill, C., Fallon, J.R., Yao, Y.M.-Y., Wallace, B.G., and McMahan, U.J. (1987). Identification of agrin, a synaptic organizing protein from Torpedo electric organ. J. Cell Biol. 105, 2471-2478.
47. Qu, Z., and Huganir, R.L. (1994). Comparison of innervation and agrin-induced tyrosine phosphorylation of the nicotinic acetylcholine receptor. J. Neurosci. 14, 6834-6841.
48. Reist, N.E., Werle, M.J., and McMahan, U.J. (1992). Agrin released by motor neurons induces the aggregation of acetylcholine receptors at neuromuscular junctions. Neuron 8, 865-868.
49. Ruegg, M.A., Tsim, K.W.K., Horton, S.E., Kroger, S., Escher, G., Gensch, E.M., and McMahan, U.J. (1992). The agrin gene encodes for a family of basal lamina proteins that differ in function and distribution. Neuron 8, 691-699.
50. Rupp, F., Payan, D.G., Magill-Solc, C., Cowan, D.M., and Scheller, R.H. (1991). Structure and expression of a rat agrin. Neuron 6, 811-823.
51. Sanes, J.R. (1995). The synaptic cleft of the neuromuscular junction. Dev. Biol. 6, 163-173.
52. Sanes, J.R., Marshall, L.M., and McMahan, U.J. (1978). Reinnervation of muscle fiber basal lamina after removal of myofibers. Differentiation of regenerating axons at original synaptic sites. J. Cell Biol. 78, 176-198.
53. Sato, T.N., Tozawa, Y., Deutsch, U., Wolburg-Buchholz, K., Fujiwara, Y., Gendron-Maguire, M., Gridley, T., Wolburg, H., Risau, W., and Qin, Y. (1995). Distinct roles of the receptor tyrosine kinase Tie1 and Tie-2 in blood vessel formation. Nature 376, 70-74.
54. Schlessinger, J., and Ullrich, A. (1992). Growth factor signaling by receptor tyrosine kinases. Neuron 9, 383-391.
55. Sealock, R., and Froehner, S.C. (1994). Dystrophin-associated proteins and synapse formation: is α-dystroglycan the agrin receptor? Cell 77, 617-619.
56. Shalaby, F., Rossant, J., Yamaguchi, T.P., Gertsenstein, M., Wu, X.F., Breitman, M.L, and Schuh, A.C. (1995). Failure of blood-island formation and vasculogenesis in Flk-1-deficient mice. Nature 376, 62-66.
57. Simon, A.M., Hoppe, P., and Burden, S.J. (1992). Spatial restriction of AChR gene expression to subsynaptic nuclei. Development 114, 545-553.
58. Snider, W.D. (1994). Functions of the neurotrophins during nervous system development: what the knockouts are teaching us. Cell 77, 627-638.
59. Son, Y.J., and Thompson, W.J. (1995). Nerve sprouting in muscle is induced and guided by processes extended by Schwann cells. Neuron 14, 133-141.
60. Sugiyama, J., Bowen, D.C., and Hall, Z.W. (1994). Dystroglycan binds nerve and muscle agrin. Neuron 13, 103-115.
61. Tsim, K.W., Ruegg, M.A., Escher, G., Kroger, S., and McMahan, U.J. (1992). cDNA that encodes active agrin. Neuron 8, 677-689.
62. Valenzuela, D.M., Stitt, T.N., DiStefano, P.S., Rojas, E., Mattsson, K., Compton, D.L., Nunez, L., Park, J.S., Stark, J.L., Gies, D.R., Thomas, S., Le Beau, 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 embryonic muscle, at the neuromuscular junction, and after injury. Neuron 15, 573-584.
63. Wallace, B.G. (1989). Agrin-induced specializations contain cytoplasmic, membrane, and extracellular matrix-associated components of the postsynaptic apparatus. J. Neurosci. 9, 1294-1302.
64. Wallace, B.G. (1994). Staurosporine inhibits agrin-induced acetylcholine receptor phosphorylation and aggregation. J. Cell Biol. 125, 661-668.
65. Wallace, B.G. (1995). Regulation of the interaction of nicotinic acetylcholine receptors with the cytoskeleton by agrin-activated protein tyrosine kinase. J. Cell Biol. 128, 1121-1129.
66. Wallace, B.G., Qu, Z., and Huganir, R.L. (1991). Agrin induces phosphorylation of the nicotinic acetylcholine receptor. Neuron 6, 869-878.
67. Zhu, X., Lai, C., Thomas, S., and Burden, S.J. (1995). Neuregulin receptors, erbB3 and erbB4, are localized at neuromuscular synapses. EMBO J. 14, 5842-5848.