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Musk signaling at the neuromuscular junction

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References

  • Apel E. D., Lewis R. M., Grady R. M., and Sanes J. R. (2000) Syne-1, a dystrophin- and Klarsicht-related protein associated with synaptic nuclei at the neuromuscular junction. J. Biol. Chem. 275, 31,986–31,995.

    Article  CAS  Google Scholar 

  • Borges L. S., Lee Y., and Ferns M. (2002) Dual role for calcium inagrin signaling and acetylcholine receptor clustering. J. Neurobiol. 50, 69–79.

    Article  PubMed  CAS  Google Scholar 

  • Campanelli, J. T., Gayer G. G., and Scheller R. H. (1996) Alternative RNA splicing that determines agrin activity regulates binding to heparin and alpha-dystroglycan. Development 122, 1663–1672.

    PubMed  CAS  Google Scholar 

  • Cartaud A., Strochlic L., Guerra M., et al. (2004) MuSK is required for anchoring acetylcholinesterase at the neuromuscular junction. J. Cell Biol. 165, 505–515.

    Article  PubMed  CAS  Google Scholar 

  • Ciani L., Krylova O., Smalley M. J., Dale T. C., and Salinas P. C. (2004) A divergent canonical WNT-signaling pathway regulates microtubule dynamics: dishevelled signals locally to stabilize microtubules. J. Cell Biol. 164, 243–253.

    Article  PubMed  CAS  Google Scholar 

  • Cotman S. L., Halfter W., and Cole G. J. (1999) Identification of extracellular matrix ligands for the heparan sulfate proteoglycan agrin. Exp. Cell Res. 249, 54–64.

    Article  PubMed  CAS  Google Scholar 

  • Daggett D. F., Cohen M. W., Stone D., Nikolics K., Rauvala H., and Peng H. B. (1996) The role of an agrin-growth factor interaction in ACh receptor clustering. Mol. Cell Neurosci 8, 272–285.

    Article  PubMed  CAS  Google Scholar 

  • Dann C. E., Hsieh J. C., Rattner A., Sharma D., Nathans J., and Leahy D. J. (2001) Insights into Wnt binding and signalling from the structures of two Frizzled cysteinerich domains. Nature 412, 86–90.

    Article  PubMed  CAS  Google Scholar 

  • DeChiara T. M., Bowen D. C., Valenzuela, D. M., et al. (1996) The receptor tyrosine kinase MuSK is required for neuromuscular junction formation in vivo. Cell 85, 501–512.

    Article  PubMed  CAS  Google Scholar 

  • Finn A. J., Feng G., and Pendergast A. M. (2003) Postsynaptic requirement for Abl kinases in assembly of the neuromuscular junction. Nat. Neurosci. 6, 717–723.

    Article  PubMed  CAS  Google Scholar 

  • Glass D. J., Bowen D. C., Stitt T. N., et al. (1996) Agrin acts via a MuSK receptor complex. Cell 85, 513–523.

    Article  PubMed  CAS  Google Scholar 

  • Grady R. M., Starr D. A., Ackerman G. L., Sanes J. R., and Han M. (2005) Syne proteins anchor muscle nuclei at the neuromuscular junction. Proc. Natl. Acad. Sci. U.S.A. 102, 4359–4364.

    Article  PubMed  CAS  Google Scholar 

  • Grow W.A., Ferns M., and Gordon H. (1999) Agrin-indepedent activation of the agrin signal transduction pathway. J. Neurobiol. 40, 356–365.

    Article  PubMed  CAS  Google Scholar 

  • Hall A. (1998) Rho GTPases and the actin cytoskeleton. Science 279, 509–514.

    Article  PubMed  CAS  Google Scholar 

  • Herbst R., Avetisova E., and Burden S. J. (2002) Restoration of synapse formation in Musk mutant mice expressing a Musk/Trk chimeric receptor. Development 129, 5449–5460.

    Article  PubMed  CAS  Google Scholar 

  • Herbst R. and Burden S. J. (2000) The juxtamembrane region of MuSK has a critical role in agrin-mediated signaling. EMBO J. 19, 67–77.

    Article  PubMed  CAS  Google Scholar 

  • Hopf C. and Hoch W. (1996) Agrin binding to alpha-dystroglycan. Domains of agrin necessary to induce acetylcholine receptor clustering are overlapping but notidentical to the alpha-dystroglycan-binding region. J. Biol. Chem. 271, 5231–5236.

    Article  PubMed  CAS  Google Scholar 

  • Hopf C. and Hoch W. (1998) Tyrosine phosphorylation of the muscle-specific kinase is exclusively induced by acetylcholine receptor-aggregating agrin fragments. Eur. J. Biochem. 253, 382–389.

    Article  PubMed  CAS  Google Scholar 

  • Krylova O., Messenger M. J., and Salinas P. C. (2000) Dishevelled-1 regulates microtubule stability: a new function mediated by glycogen synthase kinase-3beta. J. Cell Biol. 151, 83–94.

    Article  PubMed  CAS  Google Scholar 

  • Lin W., Burgess R. W., Dominguez B., Pfaff S. L., Sanes J. R., and Lee K. F. (2001) Distinct roles of nerve and muscle in postsynaptic differentiation of the neuromuscular synapse. Nature 410, 1057–1064.

    Article  PubMed  CAS  Google Scholar 

  • Logan C. Y. and Nusse R. (2004) The Wnt signaling path way in development and disease. Ann. Rev. Cell Dev. Biol. 20, 781–810.

    Article  CAS  Google Scholar 

  • Luck G., Hoch W., Hopf C., and Blottner D. (2000) Nitric oxide synthase (NOS-1) coclustered with agrin-induced AChR-specializations on cultured skeletal myotubes. Mol. Cell. Neurosci. 16, 269–281.

    Article  PubMed  CAS  Google Scholar 

  • Luo Z. G., Wang Q., Zhou J. Z., et al. (2002) Regulation of AChR clustering by Dishevelled interacting with MuSK and PAK1. Neuron 35, 489–505.

    Article  PubMed  CAS  Google Scholar 

  • Luo Z. G., Je H. S., Wang Q., et al. (2003) Implication of geranylgeranyltransferase I in synapse formation. Neuron 40, 703–717.

    Article  PubMed  CAS  Google Scholar 

  • Madhavan R., Zhao X. T., Chan F., Wu Z., and Peng H. B. (2003) The involvement of calcineurin in acetylcholine receptor redistribution in muscle. Mol. Cell. Neurosci. 23, 587–599.

    Article  PubMed  CAS  Google Scholar 

  • Manser E., Chong C., Zhao Z. S., et al. (1995) Molecular cloning of a new member of the p21-Cdc42/Racactivated kinase (PAK) family. J. Biol. Chem. 270, 25,070–25,078.

    CAS  Google Scholar 

  • Masiakowski P. and Yancopoulos G. D. (1998) The Wnt receptor CRD domain is also found in MuSK and related orphan receptor tyrosine kinases. Curr. Biol. 8, R407.

    Article  PubMed  CAS  Google Scholar 

  • Megeath L. J. and Fallon J. R. (1998) Intracellular calcium regulates agrin-induced acetylcholine receptor clustering. J. Neurosci. 18, 672–678.

    PubMed  CAS  Google Scholar 

  • Megeath L. J., Kirber M. T., Hopf C., Hoch W., and Fallon J. R. (2003) Calcium-dependent maintenance of agrin-induced postsynaptic specializations. Neuroscience 122, 659–668.

    Article  PubMed  CAS  Google Scholar 

  • Mittaud P., Marangi P. A., Erb-Vogtli S., and 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, 14,505–14,513.

    CAS  Google Scholar 

  • Mittaud P., Camilleri A. A., Willmann R., Erb-Vogtli S., Burden, S. J., and Fuhrer C. (2004) A single pulse of agrin triggers a pathway that acts to cluster acetylcholine receptors. Mol. Cell Biol. 24, 7841–7854.

    Article  PubMed  CAS  Google Scholar 

  • Mohamed A. S., Rivas-Plata K. A., Kraas J. R., Saleh, S. M., and Swope, S. L. (2001) Src-class kinases act within the agrin/MuSK pathway to regulate acetylcholine receptor phosphorylation, cytoskeletal anchoring, and clustering, J. Neurosci. 21, 3806–3818.

    PubMed  CAS  Google Scholar 

  • Montanaro, F., Gee, S. H., Jacobson, C., Lindenbaum, M. H., Froehner, S. C., and Carbonetto, S. (1998) Laminin and alpha-dystroglycan mediate acetylcholine receptor aggregation via a MuSK-independent pathway. J. Neurosci. 18, 1250–1260.

    PubMed  CAS  Google Scholar 

  • O'Toole, J. J., Deyst, K. A., Bowe, M. A., Nastuk, M. A., McKechnie, B. A., and Fallon, J. R. (1996) Alternative splicing of agrin regulates its binding to heparin alphadystroglycan, and the cell surface. Proc. Natl. Acad. Sci. U. S. A. 93, 7369–7374.

    Article  PubMed  Google Scholar 

  • Packard M., Koo, E. S., Gorczyca, M., Sharpe J., Cumberledge S., and Budnik V. (2002) The Drosophila Wnt, wingless, provides an essential signal for pre-and postsynaptic differentiation. Cell 111, 319–330.

    Article  PubMed  CAS  Google Scholar 

  • Parkhomoyskiy N., Kammesheidt A., and Martin P. T. (2000) N-acetyllactosamine and the CT carbohydrate antigen mediate agrin-dependent activation of MuSK and acetylcholine receptor clustering in skeletal muscle. Mol. Cell. Neurosci. 15, 380–397.

    Article  Google Scholar 

  • Peng H. B., Ali A. A., Dai Z., Daggett D. F., Raulo E., and Rauvala H. (1995) The role of heparin-binding growth-associated molecule (HB-GAM) in the postsynaptic induction in cultured muscle cells. J. Neurosci. 15, 3027–3038.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Rauvala H. and Peng H. B. (1997) HB-GAM (heparin-binding growth-associated molecule) and heparin-type glycans in the development and plasticity of neuron-target contacts. Prog. Neurobiol. 52, 127–144.

    Article  PubMed  CAS  Google Scholar 

  • Sanes J. R. and Lichtman J. W. (2001) Induction, assembly, maturation and maintenance of a postsynaptic apparatus. Nat. Rev. Neurosci. 2, 791–805.

    Article  PubMed  CAS  Google Scholar 

  • Sanes J. R. and Lichtman J. W. (1999) Development of the vetebrate neuromuscular junction. Ann. Rev. Neurosci. 22, 389–442.

    Article  PubMed  CAS  Google Scholar 

  • Sharma S. K. and Wallace B. G. (2003) Lithium inhibits a late step in agrin-induced AChR aggregation. J. Neurobiol. 54, 346–357.

    Article  PubMed  CAS  Google Scholar 

  • Smith C. L., Mittaud P., Prescott E. D., Fuhrer C., and Burden S. J. (2001) Src, Fyn, and Yes are not required for neuromuscular synapse formation but are necessary forstabilization of agrin-induced clusters of acetylcholine receptors. J. Neurosci. 21, 3151–3160.

    PubMed  CAS  Google Scholar 

  • Storms S. D., Kim A. C., Tran B. H., Cole G. J., and Murray B. A. (1996) NCAM-mediated adhesion of transfected cells to agrin. Cell Adhes. Commun. 3, 497–509.

    PubMed  CAS  Google Scholar 

  • Strochlic L., Cartaud A., Labas V., Hoch W., Rossier J., and Cartaud J. (2001) MAGI-1c: a synaptic MAGUK interacting with muSK at the vertebrate neuromuscular junction. J. Cell Biol. 153, 1127–1132.

    Article  PubMed  CAS  Google Scholar 

  • Sugiyama J. E., Glass D. J., Yancopoulos G. D., and Hall Z. W. (1997) Laminin-induced acetylcholine receptor clustering: an alternative pathway. J. Cell. Biol. 139, 181–191.

    Article  PubMed  CAS  Google Scholar 

  • Wang, J., Jing Z., Zhang L., et al. (2003) Regulation of acetylcholine receptor clustering by the tumor suppressor APC. Nat. Neurosci. 6, 1017–1018.

    Article  PubMed  CAS  Google Scholar 

  • Watty A. and Burden S. J. (2002) MuSK glycosylation restrains MuSK activation and acetylcholine receptor clustering. J. Biol. Chem. 277, 50,457–50,462.

    Article  CAS  Google Scholar 

  • Weston C., Yee B. Hod E., and Prives J. (2000) Agrin-induced Acetylcholine receptor clustering is mediated by the small guanosine triphosphatases Rac and Cdc42 J. Cell. Biol. 150, 205–212.

    Article  PubMed  CAS  Google Scholar 

  • Weston C., Gordon C., Teressa G., Hod E., Ren X. D., and Prives J. (2003) Cooperative regulation by Rac and Rho of agrin-induced acetylcholine receptor clustering in muscle cells. J. Biol. Chem. 278, 6450–6455.

    Article  PubMed  CAS  Google Scholar 

  • Xu Y. K. and Nusse R. (1998) The Frizzled CRD domain is conserved in diverse proteins including several receptor tyrosine kinases. Curr. Biol. 8, R405-R406.

    Article  PubMed  CAS  Google Scholar 

  • Yancopoulos G. D., Maisonpierre P. C., Ip N. Y., et al. (1990) Neurotrophic factors, their receptors, and the signal transduction pathways they activate. Cold Spring Harb. Symp. Quant. Biol. 55, 371–379.

    PubMed  CAS  Google Scholar 

  • Yang X., Arber S., William C., et al. (2001) Patterning of muscle acetylcholine receptor gene expression in the absence of motor innervation. Neuron 30, 399–410.

    Article  PubMed  CAS  Google Scholar 

  • Zhou H., Muramatsu T., Halfter W., Tsim K. W., and Peng H. B. (1997) A role of midkine in the development of the neuromuscular junction. Mol. Cell Neurosci. 10, 56–70.

    Article  PubMed  CAS  Google Scholar 

  • Zhou H., Glass D. J., Yancopoulos G. D., and Sanes J. R. (1999) Distinct domains of MuSK mediate its abilities to induce and to associate with postsynaptic specializations. J. Cell Biol. 146, 1133–1146.

    Article  PubMed  CAS  Google Scholar 

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Correspondence to Lin Mei.

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Wang, Q., Zhang, B., Xiong, WC. et al. Musk signaling at the neuromuscular junction. J Mol Neurosci 30, 223–226 (2006). https://doi.org/10.1385/JMN:30:1:223

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