Fluorescent Imaging of Nicotinic Receptors During Neuromuscular Junction Development

  • Zhengshan Dai
  • H. Benjamin Peng
Part of the Methods in Pharmacology and Toxicology book series (MIPT)


Synaptic transmission at the vertebrate neuromuscular junction (NMJ) is accomplished by activity-dependent release of the neurotransmitter acetylcholine from the motor terminal and its detection by nicotinic acetylcholine receptors (AChRs) residing in the postsynaptic membrane of the skeletal muscle cell. The vesicular release at the nerve terminal is a highly efficient process that ensures the exocytosis of several hundred quanta upon each nerve impulse. The high fidelity of the ACh detection is based on the fact that AChRs are clustered to extremely high density at the postsynaptic membrane. Thus, the hallmark of NMJ development is the temporal and spatial registration of the vesicular release mechanism and the postsynaptic AChR clustering.


Skeletal Muscle Cell Postsynaptic Membrane AChR Cluster Culture Muscle Cell Phenylarsine Oxide 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. 1.
    Lee, C. Y., Chang, S. L., Kau, S. T., and Luh, S.-H. (1972) Chromatographic separation of the venom of Bungarus multicinctus and characterization of its components. J. Chromatogr. 72, 71–82.PubMedCrossRefGoogle Scholar
  2. 2.
    McCarthy, M. P., Earnest, J. P., Young, E. F., Choe, S., and Stroud, R. M. (1986) The molecular neurobiology of the acetylcholine receptor. Ann. Rev. Neurosci. 9, 383–413.PubMedCrossRefGoogle Scholar
  3. 3.
    Schuetze, S. M. and Role, L. W. (1987) Developmental regulation of nicotinic acetylcholine receptors. Ann. Rev. Neurosci. 10, 403–457.PubMedCrossRefGoogle Scholar
  4. 4.
    Witzemann, V., Brenner, H.-R., and Sakmann, B. (1991) Neural factors regu-late AChR subunit mRNAs at rat neuromuscular synapses. J. Cell Biol. 114, 125–141.PubMedCrossRefGoogle Scholar
  5. 5.
    Fertuck, H. C. and Salpeter, M. M. (1974) Localization of acetylcholine receptor by 125I-labeled α-bungarotoxin binding at mouse motor endplates. Proc. Natl. Acad. Sci. USA 71, 1376–1378.PubMedCrossRefGoogle Scholar
  6. 6.
    Anderson, M. J. and Cohen, M. W. (1974) Fluorescent staining of acetylcholine receptors in vertebrate skeletal muscle. J. Physiol. (Lond.) 237, 385–400.Google Scholar
  7. 7.
    Ravdin, P. and Axelrod, D. (1977) Fluorescent tetramethyl rhodamine derivatives of alpha-bungarotoxin: preparation, separation and characterization. Anal. Biochem. 80, 585–592.PubMedCrossRefGoogle Scholar
  8. 8.
    Anderson, M. J. and Cohen, M. W. (1977) Nerve-induced and spontaneous redistribution of acetylcholine receptors on cultured muscle cells. J. Physiol. (Lond.) 268, 757–773.Google Scholar
  9. 9.
    Frank, E. and Fischbach, G. D. (1979) Early events in neuromuscular junction formation in vitro. J. Cell Biol. 83, 143–158.PubMedCrossRefGoogle Scholar
  10. 10.
    Sytkowski, A. J., Vogel, Z., and Nirenberg, M. W. (1973) Development of acetylcholine receptor clusters on cultured muscle cells. Proc. Natl. Acad. Sci. USA 70, 270–274.PubMedCrossRefGoogle Scholar
  11. 11.
    Bloch, R. J. and Pumplin, D. W. (1988) Molecular events in synaptogenesis: nerve-muscle adhesion and postsynaptic differentiation. Am. J. Physiol. 254, C345–C364.PubMedGoogle Scholar
  12. 12.
    Peng, H. B. (1987) Development of the neuromuscular junction in tissue culture. CRC Crit. Rev. Anat. Sci. 1, 91–131.Google Scholar
  13. 13.
    Weldon, P. R., Moody-Corbett, F., and Cohen, M. W. (1981) Ultrastructure of sites of cholinesterase activity on amphibian embryonic muscle cells cultured without nerve. Dev. Biol. 84, 341–350.PubMedCrossRefGoogle Scholar
  14. 14.
    Bekoff, A. and Betz, W. J. (1976) Acetylcholine hot spots: development on myotubes cultured from aneural limb buds. Science 193, 915–917.PubMedCrossRefGoogle Scholar
  15. 15.
    Ko, P. K., Anderson, M. J., and Cohen, M. W. (1977) Denervated skeletal muscle fibers develop discrete patches of high acetylcholine receptor density. Science 196, 540–542.PubMedCrossRefGoogle Scholar
  16. 16.
    Sohal, G. S. (1988) Development of postsynaptic-like specializations of the neuromuscular synapse in the absence of motor nerve. Int. J. Dev. Neurosci. 6, 553–565.PubMedCrossRefGoogle Scholar
  17. 17.
    Cohen, I., Rimer, M., Lomo, T., and McMahan, U. J. (1997) Agrin-induced postsynaptic-like apparatus in skeletal muscle fibers in vivo. Mol. Cell. Neurosci. 9, 237–253.PubMedCrossRefGoogle Scholar
  18. 18.
    Meier, Th., Hauser, D. M., Chiquet, M., Landmann, L., Ruegg, M. A., and Brenner, H. R. (1997) Neural agrin induces ectopic postsynaptic specializations in innervated muscle fibers. J. Neurosci. 17, 6534–6544.PubMedGoogle Scholar
  19. 19.
    Anderson, M. J., Cohen, M. W., and Zorychta, E. (1977) Effects of innervation on the distribution of acetylcholine receptors on cultured muscle cells. J. Physiol. (Lond.) 268, 731–756.Google Scholar
  20. 20.
    Buchanan, J., Sun, Y., and Poo, M.-M. (1989) Studies of nerve-muscle interactions in Xenopus cell culture: fine structure of early functional contacts. J. Neurosci. 9, 1540–1554.PubMedGoogle Scholar
  21. 21.
    Nakajima, Y., Kidokoro, Y., and Klier, F. G. (1980) The development of functional neuroumuscular junctions in vitro: an ultrastructural and physiological study. Dev. Biol. 77, 52–72.PubMedCrossRefGoogle Scholar
  22. 22.
    Peng, H. B., Nakajima, Y., and Bridgman, P. C. (1980) Development of the postsynaptic membrane in Xenopus neuromuscular cultures observed by freeze-fracture and thin-section electron microscopy. Brain Res. 196, 11–31.PubMedCrossRefGoogle Scholar
  23. 23.
    Cohen, M. W. and Weldon, P. R. (1980) Localization of acetylcholine receptors and synaptic ultrastructure at nerve-muscle contacts in culture: dependence on nerve type. J. Cell Biol. 86, 388–401.PubMedCrossRefGoogle Scholar
  24. 24.
    Role, L. W., Matossian, V. R., O’Brien, R. J., and Fischbach, G. D. (1985) On the mechanism of acetylcholine receptor accumulation at newly formed synapses on chick myotubes. J. Neurosci. 5, 2197–2204.PubMedGoogle Scholar
  25. 25.
    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.PubMedCrossRefGoogle Scholar
  26. 26.
    McMahan, U. J., Horton, S. E., Werle, M. J., Honig, L. S., Kroger, S., Ruegg, M. A., and Escher, G. (1992) Agrin isoforms and their role in synaptogenesis. Curr. Opin. Cell Biol. 4, 869–874.PubMedCrossRefGoogle Scholar
  27. 27.
    Ruegg, M. A. and Bixby, J. L. (1998) Agrin orchestrates synaptic differentiation at the vertebrate neuromuscular junction. Trends Neurosci. 21, 22–27.PubMedCrossRefGoogle Scholar
  28. 28.
    Tsen, G., Halfter, W., Kroger, S., and Cole, G. J. (1995) Agrin is a heparan sulfate proteoglycan. J. Biol. Chem. 270, 3392–3399.PubMedCrossRefGoogle Scholar
  29. 29.
    Cole, G. J. and Halfter, W. (1996) Agrin: an extracellular matrix heparan sulfate proteoglycan involved in cell interactions and synaptogenesis. Persp. Dev. Neurobiol. 314, 359–371.Google Scholar
  30. 30.
    Groffen, A. J., Ruegg, M. A., Dijkman, H., van de Velden, T. J., Buskens, C. A., Van den Born, J., et al. (1998) Agrin is a major heparan sulfate proteoglycan in the human glomerular basement membrane. J. Histochem. Cytochem. 46, 19–28.PubMedGoogle Scholar
  31. 31.
    Raats, C. J. I., Bakker, M. A. H., Hoch, W., Tamboer, W. P. M., Groffen, A. J. A., Van den Heuvel, L. P. W. J., et al. (1998) Differential expression of agrin in renal basement membranes as revealed by domain-specific antibodies. J. Biol. Chem. 273, 17,832–17,838.PubMedCrossRefGoogle Scholar
  32. 32.
    Bowe, M. A. and Fallon, J. R. (1995) The role of agrin in synapse formation. Ann. Rev. Neurosci. 18, 443–462.PubMedCrossRefGoogle Scholar
  33. 33.
    Hall, Z. W. and Sanes, J. R. (1993) Synaptic structure and development: the neuromuscular junction. Neuron 10(Suppl.), 99–121.Google Scholar
  34. 34.
    Gautam, M., Noakes, P. G., Moscoso, L., Rupp, F., Scheller, R. H., Merlie, J. P., and Sanes, J. R. (1996) Defective neuromuscular synaptogenesis in agrindeficient mutant mice. Cell 85, 525–535.PubMedCrossRefGoogle Scholar
  35. 35.
    Sanes, J. R. (1997) Genetic analysis of postsynaptic differentiation at the vertebrate neuromuscular junction. Curr. Opin. Neurobiol. 7, 93–100.PubMedCrossRefGoogle Scholar
  36. 36.
    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.PubMedCrossRefGoogle Scholar
  37. 37.
    Nastuk, M. A., Lieth, E., Ma, J., Cardasis, C. A., Moynihan, E. B., McKechnie, B. A., and Fallon, J. R. (1991) The putative agrin receptor binds ligand in a calcium-dependent manner and aggregates during agrin-induced acetylcholine receptor clustering. Neuron 7, 807–818.PubMedCrossRefGoogle Scholar
  38. 38.
    Baker, L. P. and Peng, H. B. (1995) Induction of acetylcholine receptor cluster formation by local application of growth factors in cultured Xenopus muscle cells. Neurosci. Lett. 185, 135–138.PubMedCrossRefGoogle Scholar
  39. 39.
    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.PubMedGoogle Scholar
  40. 40.
    Peng, H. B. and Cheng, P.-C. (1982) Formation of postsynaptic specializations induced by latex beads in cultured muscle cells. J. Neurosci. 2, 1760–1774.PubMedGoogle Scholar
  41. 41.
    Peng, H. B., Cheng, P.-C., and Luther, P. W. (1981) Formation of ACh receptor clusters induced by positively charged latex beads. Nature 292, 831–834.PubMedCrossRefGoogle Scholar
  42. 42.
    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.PubMedCrossRefGoogle Scholar
  43. 43.
    Zhou, H., Muramatsu, T., Halfter, W., Tsim, K. W. K., and Peng, H. B. (1997) A role of midkine in the development of the neuromuscular junction. Mol. Cell. Neurosci. 10, 56–70.PubMedCrossRefGoogle Scholar
  44. 44.
    Luther, P. W. and Peng, H. B. (1985) Membrane-related specializations associated with acetylcholine receptor aggregates induced by electric fields. J. Cell Biol. 100, 235–244.PubMedCrossRefGoogle Scholar
  45. 45.
    Orida, N. and Poo, M.-M. (1978) Electrophoretic movement and localisation of acetylcholine receptors in the embryonic muscle cell membrane. Nature 275, 31–35.PubMedCrossRefGoogle Scholar
  46. 46.
    Peng, H. B., Baker, L. P., and Dai, Z. (1993) A role of tyrosine phosphorylation in the formation of acetylcholine receptor clusters induced by electric fields in cultured Xenopus muscle cells. J. Cell Biol. 120, 197–204.PubMedCrossRefGoogle Scholar
  47. 47.
    Fang, K. S., Ionides, E., Oster, G., Nuccitelli, R., and Isseroff, R. R. (1999) Epidermal growth factor receptor relocalization and kinase activity are necessary for directional migration of keratinocytes in DC electric fields. J. Cell Sci. 112(Pt 12), 1967–1978.PubMedGoogle Scholar
  48. 48.
    Burden, S. J. (1985) The subsynaptic 43kDa protein is concentrated at developing nerve-muscle synapses in vitro. Proc. Natl. Acad. Sci. USA 82, 8270–8273.PubMedCrossRefGoogle Scholar
  49. 49.
    LaRochelle, W. J. and Froehner, S. C. (1986) Determination of the tissue distributions and relative concentrations of the postsynaptic 43-kDa protein and the acetylcholine receptor in Torpedo. J. Biol. Chem. 261, 5270–5274.PubMedGoogle Scholar
  50. 50.
    Peng, H. B. and Froehner, S. C. (1985) Association of the postsynaptic 43K protein with newly formed acetylcholine receptor clusters. J. Cell Biol. 100, 1698–1705.PubMedCrossRefGoogle Scholar
  51. 51.
    Sealock, R., Wray, B. E., and Froehner, S. C. (1984) Ultrastructural localization of the Mr 43,000 protein and the acetylcholine receptor in Torpedo postsynaptic membrane using monoclonal antibodies. J. Cell Biol. 98, 2239–2244.PubMedCrossRefGoogle Scholar
  52. 52.
    Sobel, A., Weber, M., and Changeux, J.-P. (1977) Large-scale purification of the acetylcholine-receptor protein in its membrane-bound and detergent extracted forms from Torpedo marmorata electric organ. Eur. J. Biochem. 80, 215–224.PubMedCrossRefGoogle Scholar
  53. 53.
    Burden, S. J., Depalma, R. L., and Gottesman, G. S. (1983) Crosslinking of proteins in acetylcholine receptor-rich membranes: association between the beta-subunit and the 43 kd subsynaptic protein. Cell 35, 687–692.PubMedCrossRefGoogle Scholar
  54. 54.
    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.PubMedCrossRefGoogle Scholar
  55. 55.
    Phillips, W. D., Maimone, M. M., and Merlie, J. P. (1991) Mutagenesis of the 43-kD postsynaptic protein defines domains involved in plasma membrane targeting and AChR clustering. J. Cell Biol. 115, 1713–1723.PubMedCrossRefGoogle Scholar
  56. 56.
    Yu, X.-M. and Hall, Z. W. (1994) The role of the cytoplasmic domains of individual subunits of the acetylcholine receptor in 43 kDa protein-induced clustering in COS cells. J. Neurosci. 14, 785–795.PubMedGoogle Scholar
  57. 57.
    Porter, S. and Froehner, S. C. (1983) Characterization of the Mr 43,000 proteins associated with acetylcholine receptor-rich membranes. J. Biol. Chem. 258, 10034–10040.PubMedGoogle Scholar
  58. 58.
    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.PubMedCrossRefGoogle Scholar
  59. 59.
    Dai, Z., Scotland, P. B., Froehner, S. C., and Peng, H. B. (1996) Association of phosphotyrosine with rapsyn expressed in Xenopus embryonic cells. Neuroreport 7, 657–661.PubMedCrossRefGoogle Scholar
  60. 60.
    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.PubMedCrossRefGoogle Scholar
  61. 61.
    Phillips, W. D., Kopta, C., Blount, P., Gardner, P. D., Steinbach, J. H., and Merlie, J. P. (1991) ACh receptor-rich membrane domains organized in fibroblasts by recombinant 43-kilodalton protein. Science 251, 568–570.PubMedCrossRefGoogle Scholar
  62. 62.
    Musil, L. S., Carr, C., Cohen, J. B., and Merlie, J. P. (1988) Acetylcholine receptor-associated 43K protein contains covalently bound myristate. J. Cell Biol. 107, 1113–1121.PubMedCrossRefGoogle Scholar
  63. 63.
    Ramarao, M. K. and Cohen, J. B. (1998) Mechanism of nicotinic acetylcholine receptor cluster formation by rapsyn. Proc. Natl. Acad. Sci. USA 95, 4007–4012.PubMedCrossRefGoogle Scholar
  64. 64.
    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.CrossRefGoogle Scholar
  65. 65.
    Axelrod, D. (1980) Crosslinkage and visualization of acetylcholine receptors on myotubes with biotinylated α-bungarotoxin and fluorescent avidin. Proc. Natl. Acad. Sci. USA 77, 4823–4827.PubMedCrossRefGoogle Scholar
  66. 66.
    Baker, L. P. and Peng, H. B. (1993) Tyrosine phosphorylation and acetylcholine receptor cluster formation in cultured Xenopus muscle cells. J. Cell Biol. 120, 185–195.PubMedCrossRefGoogle Scholar
  67. 67.
    Dai, Z. and Peng, H. B. (1999) The dissociation of ACh receptor and phosphotyrosine cluster formation and dispersal induced by signals for synaptotgenesis. Soc. Neurosci. Abstr. 25, 239.Google Scholar
  68. 68.
    Peng, H. B. and Phelan, K. A. (1984) Early cytoplasmic specialization at the presumptive acetylcholine receptor cluster: a meshwork of thin filaments. J. Cell Biol. 99, 344–349.PubMedCrossRefGoogle Scholar
  69. 69.
    Axelrod, D., Ravdin, P., Koppel, D. E., Schlessinger, J., Webb, W. W., Elson, E. L., and Podleski, T. R. (1976) Lateral motion of fluorescently labeled acetylcholine receptors in membranes of developing muscle fibers. Proc. Natl. Acad. Sci. USA 73, 4954–4958.CrossRefGoogle Scholar
  70. 70.
    Kidokoro, Y. and Brass, B. (1985) Redistribution of acetylcholine receptors during neuromuscular junction formation in Xenopus cultures. J. Physiol. (Paris) 80, 212–220.Google Scholar
  71. 71.
    Peng, H. B., Zhao, D.-Y., Xie, M.-Z., Shen, Z., and Jacobson, K. (1989) The role of lateral migration in the formation of acetylcholine receptor clusters induced by basic polypeptide-coated latex beads. Dev. Biol. 131, 197–206.PubMedCrossRefGoogle Scholar
  72. 72.
    Edwards, C. and Frisch, H. L. (1976) A model for the localization of acetylcholine receptors at the muscle endplate. J. Neurobiol. 7, 377–381.PubMedCrossRefGoogle Scholar
  73. 73.
    Qu, Z., Moritz, E., and Huganir, R. L. (1990) Regulation of tyrosine phosphorylation of the nicotinic acetylcholine receptor at the rat neuromuscular junction. Neuron 4, 367–378.PubMedCrossRefGoogle Scholar
  74. 74.
    Wallace, B. G., Qu, Z., and Huganir, R. L. (1991) Agrin induces phosphorylation of the nicotinic acetylcholine receptor. Neuron 6, 869–878.PubMedCrossRefGoogle Scholar
  75. 75.
    DeChiara, T. M., Bowen, D. C., Valenzuela, D. M., Simmons, M. V., Poueymirou, W. T., Thomas, S., et al. (1996) The receptor tyrosine kinase MuSK is required for neuromuscular junction formation in vivo. Cell 85, 501–512.PubMedCrossRefGoogle Scholar
  76. 76.
    Glass, D. J., Bowen, D. C., Stitt, T. N., Radziejewski, C., Bruno, J., Ryan, T. E., et al. (1996) Agrin acts via a MuSK receptor complex. Cell 85, 513–523.PubMedCrossRefGoogle Scholar
  77. 77.
    Besser, J., Zahalka, M. A., and Ullrich, A. (1996) Exclusive expression of the receptor tyrosine kinase MDK4 in skeletal muscle and the decidua. Mech. Dev. 59, 41–52.PubMedCrossRefGoogle Scholar
  78. 78.
    Fu, A. K. Y., Smith, F. D., Zhou, H., Chu, A. H., Tsim, K. W. K., Peng, B. H., and Ip, N. Y. (1999) Xenopus muscle-specific kinase: molecular cloning and prominent expression in neural tissues during early embryonic development. Eur. J. Neurosci. 11, 373–382.PubMedCrossRefGoogle Scholar
  79. 79.
    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.PubMedGoogle Scholar
  80. 80.
    Valenzuela, D. M., Stitt, T. N., DiStefano, P. S., Rojas, E., Mattsson, K., Compton, D. L., et al. (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.PubMedCrossRefGoogle Scholar
  81. 81.
    Sealock, R., Butler, M. H., Kramarcy, N. R., Gao, K.-X., Murnane, A. A., Douville, K., and Froehner, S. C. (1991) Localization of dystrophin relative to acetylcholine receptor domains in electric tissue and adult and cultured skeletal muscle. J. Cell Biol. 113, 1133–1144.PubMedCrossRefGoogle Scholar
  82. 82.
    Deconinck, A. E., Rafael, J. A., Skinner, J. A., Brown, S. C., Potter, A. C., Metzinger, L., et al. (1997) Utrophin-dystrophin-deficient mice as a model for Duchenne muscular dystrophy. Cell 90, 717–727.PubMedCrossRefGoogle Scholar
  83. 83.
    Grady, R. M., Teng, H. B., Nichol, M. C., Cunningham, J. C., Wilkinson, R. S., and Sanes, J. R. (1997) Skeletal and cardiac myopathies in mice lacking utrophin and dystrophin: a model for Duchenne muscular dystrophy. Cell 90, 729–738.PubMedCrossRefGoogle Scholar
  84. 84.
    Bloch, R. J. (1986) Actin at receptor-rich domains of isolated acetylcholine receptor clusters. J. Cell Biol. 102, 1447–1458.PubMedCrossRefGoogle Scholar
  85. 85.
    Jasmin, B. J., Changeux, J.-P., and Cartaud, J. (1990) Compartmentalization of cold-stable and acetylated microtubules in the subsynaptic domain of chick skeletal muscle fibre. Nature 344, 673–675.PubMedCrossRefGoogle Scholar
  86. 86.
    Peng, H. B., Xie, H., and Dai, Z. (1997) The association of cortactin with developing neuromuscular specializations. J. Neurocytol. 26, 637–650.PubMedCrossRefGoogle Scholar
  87. 87.
    Peng, H. B. and Dai, Z. (1999) The role of actin polymerization in the formation of ACh receptor clusters in muscle cells. Soc. Neurosci. Abstr. 25, 239.Google Scholar
  88. 88.
    Koenig, M., Monaco, A. P., and Kunkel, L. M. (1988) The complete sequence of dystrophin predicts a rod-shaped cytoskeletal protein. Cell 53, 219–228.PubMedCrossRefGoogle Scholar
  89. 89.
    Rybakova, I. N., Amann, K. J., and Ervasti, J. M. (1996) A new model for the interaction of dystrophin with F-actin. J. Cell Biol. 135, 661–672.PubMedCrossRefGoogle Scholar
  90. 90.
    Apel, E. D., Glass, D. J., Moscoso, L. M., Yancopoulos, G. D., and Sanes, J. R. (1997) Rapsyn is required for MuSK signaling and recruits synaptic components to a MuSK-containing scaffold. Neuron 18, 623–635.PubMedCrossRefGoogle Scholar
  91. 91.
    Balice-Gordon, R. J. and Lichtman, J. W. (1994) Long-term synapse loss induced by focal blockade of postsynaptic receptors. Nature 372, 519–524.PubMedCrossRefGoogle Scholar
  92. 92.
    Daggett, D. F., Stone, D., Peng, H. B., and Nikolics, K. (1996) Full-length agrin isoform activities and binding site distributions on cultured Xenopus muscle cells. Mol. Cell. Neurosci. 7, 75–88.PubMedCrossRefGoogle Scholar
  93. 93.
    Dai, Z. and Peng, H. B. (1998) A role of tyrosine phosphatase in acetylcholine receptor cluster dispersal and formation. J. Cell Biol. 141, 1613–1624.PubMedCrossRefGoogle Scholar
  94. 94.
    Kuromi, H. and Kidokoro, Y. (1984) Nerve disperses preexisting acetylcholine receptor clusters prior to induction of receptor. Dev. Biol. 103, 53–61.PubMedCrossRefGoogle Scholar

Copyright information

© Humana Press Inc., Totowa, NJ 2001

Authors and Affiliations

  • Zhengshan Dai
    • 1
  • H. Benjamin Peng
    • 1
  1. 1.Department of Cell Biology and AnatomyUniversity of North Carolina at Chapel HillChapel Hill

Personalised recommendations