Skip to main content
SpringerLink
Log in

Formation of the Vertebrate Neuromuscular Junction

  • Chapter
The Cellular Basis of Morphogenesis

Part of the book series: Developmental Biology ((DEBO,volume 2))

  • 135 Accesses

Abstract

The formation of the neuromuscular junction (NMJ) is an example of establishment of contact between unlike cells—nerve and muscle—that results in functional interaction between them. This chapter focuses on the establishment of contact, the morphogenesis of the NMJ, the acquisition of functional competence, and the regulation of these processes at the cellular level. This chapter is not an exhaustive review of the area; rather, coverage is restricted to the development of the NMJs in three organisms: rat, chick, and the amphibian Xenopus laevis. The exact sequence of events leading to the formation of a NMJ will in the end be unique to that junction. However, general principles will apply to the development of all NMJs. The aim of the present study is to describe the general features common to the development of the junctions of these three preparations. The formation of the NMJ, including studies pertaining to the effects of denervation and regeneration, has also been recently reviewed by Bennett (1983).

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Alcerno, B. B., 1965, The nature of the earliest spontaneous activity of the chick embryo, J. Embryol. Exp. MorphoJ. 13: 255–266.

    Google Scholar 

  • Anderson, M. J., and Cohen, M. W., 1977, Nerve-induced and spontaneous redistribution of acetylcholine receptors on cultured muscle cells, J. Physiol. ( Lond.J 268: 757–773.

    CAS  Google Scholar 

  • Anderson, M. J., and Fambrough, D. M., 1983, Aggregates of acetylcholine receptors are associated with plaques of a basal lamina heparan sulfate proteoglycan on the surface of skeletal muscle fibers, J. Cell Biol. 97: 1396–1411.

    PubMed  CAS  Google Scholar 

  • Anderson, C. R., and Stevens, C. F., 1973, Voltage clamp analysis of acetylcholine produced end- plate current fluctuations at frog neuromuscular junction, J. Physiol. (Lond.) 235: 655–691.

    CAS  Google Scholar 

  • Anderson, M. J., Kidokoro, Y., and Gruener, R., 1979, Correlation between acetylcholine receptor localization and spontaneous synaptic potentials in cultures of nerve and muscle, Brain Bes. 166: 185–190.

    CAS  Google Scholar 

  • Anderson, M. J., Cohen, M. W., and Zorychta, E., 1977, Effects of innervation on the distribution of acetylcholine receptors on cultured amphibian muscle cells, J. Physiol. ( Lond.) 268: 731–756.

    CAS  Google Scholar 

  • Atsumi, S., 1977, Development of neuromuscular junctions of fast and slow muscles in the chick embryo: A light and electron microscope study, J. Neurocytol. 6: 691–709.

    PubMed  CAS  Google Scholar 

  • Axelrod, D., 1981, Cell-substrate contacts illuminated by total internal reflection fluorescence, J. Cell Biol 89: 141–145.

    PubMed  CAS  Google Scholar 

  • Axelrod, D., Ravdin, P., Koppel, D. E., Schlessinger, J., Webb, W. W., Elson, E. L., and Podleski, T. R., 1976, Lateral motion of fluorescently labelled acetylcholine receptors in membranes of developing muscle cells, Proc. Natl. Acad. Sci. USA 73: 4594–4598.

    PubMed  CAS  Google Scholar 

  • Axelrod, D., Ravdin, P., and Podleski, T. R., 1978, Control of acetylcholine receptor mobility and distribution in cultured muscle membranes, Biochim. Biophys. Acta 511: 23–38.

    PubMed  CAS  Google Scholar 

  • Barnard, E. A., Lai, J., and Pizzey, J., 1984, Synaptic and extrasynaptic forms of acetylcholinesterase in skeletal muscles: Variation with fiber type and functional considerations, in: Neuromuscular Diseases ( G. Serratrice, D. Cros, C. Desnuelle, J.-L. Gastaut, J.-F. Pellisier, J. Pouget, and A. Schiano, eds.), pp. 455–463, Raven Press, New York.

    Google Scholar 

  • Bekoff, A., and Betz, W. H., 1976, Acetylcholine hotspots: Development on myotubes cultured from aneural limb buds, Science 193: 915–917.

    PubMed  CAS  Google Scholar 

  • Bennett, M. R., 1983, Development of neuromuscular synapses, Physiol. Rev. 63: 915 - 1048.

    PubMed  CAS  Google Scholar 

  • Bennett, M. R., and Pettigrew, A. G., 1974, The formation of synapses in striated muscle during development, J. Physiol. (Lond.) 241: 515–545.

    CAS  Google Scholar 

  • Betz, W., 1976, The formation of synapses between chick embryo skeletal muscle and ciliary ganglia grown in vitro,]. PhysioJ. (Lond.) 254: 63–73.

    CAS  Google Scholar 

  • Betz, W., and Sakmann, B., 1973, Effects of proteolytic enzymes on function and structure of frog neuromuscular junction, J. Physiol. (Lond.) 230: 673–688.

    CAS  Google Scholar 

  • Betz, H., Bourgeois, J.-P., and Changeux, J.-P., 1980, Evolution of cholinergic proteins in developing slow and fast skeletal muscle in chick embryo, J. Physiol. (Lond.) 302: 197–218.

    CAS  Google Scholar 

  • Bevan, S., and Steinbach, J. H., 1977, The distribution of alpha-bungarotoxin in binding sites on mammalian skeletal muscle developing in vivo, J. Physiol. (Lond.) 267: 195–213.

    CAS  Google Scholar 

  • Bevan, S., and Steinbach, J. H., 1977, The distribution of alpha-bungarotoxin in binding sites on mammalian skeletal muscle developing in vivo, J. Physiol. (Lond.) 267: 195–213.

    Google Scholar 

  • Blackshaw, S., and Warner, A., 1976, Onset of acetylcholine sensitivity and endplate activity in developing myotome muscles of Xenopus, Nature (Lond.) 262: 217–218.

    CAS  Google Scholar 

  • Bloch, R., and Geiger, B., 1980, Localization of acetylcholine receptor clusters in areas of cell- substrate contact in cultures of rat myotubes, Cell 211: 25–35.

    Google Scholar 

  • Bowden, R., and Duchen, L. W., 1976, The anatomy and pathology of the neuromuscular junction, in: Neuromuscular function ( E. Zaimis, ed.), pp. 1–92, Springer-Verlag, New York.

    Google Scholar 

  • Braithwaite, A. W., and Harris, A. J., 1979, Neural influence on acetylcholine receptor clusters in embryonic development of skeletal muscle, Nature (Lond.) 279: 549–551.

    CAS  Google Scholar 

  • Brehm, P., Steinbach, J. H., and Kidokoro, Y., 1982, Channel open time of acetylcholine receptors on Xenopus muscle cells in dissociated cell cultures, Dev. Biol. 91: 93–102.

    PubMed  CAS  Google Scholar 

  • Brehm, P., Moody-Corbett, F., and Kidokoro, Y., 1983a, Developmental alterations in acetylcholine receptor channel properties proceed in the absence of innervation, Neurosci. Abs. 9: 1180.

    Google Scholar 

  • Brehm, P., Yeh, E., Patrick, G., and Kidokoro, Y., 1983b, Metabolism of acetylcholine receptors on embryonic amphibian muscle, J. Neurosci. 3: 101–107.

    PubMed  CAS  Google Scholar 

  • Brehm, P., Kullberg, R., and Moody-Corbett, F., 1984a, Properties of non-junctional acetylcholine receptor channels on innervated muscle of Xenopus laevis, J. Physiol. (Lond.) 350: 631–648.

    CAS  Google Scholar 

  • Brehm, P., Kidokoro, Y., and Moody-Corbett, F., 1984b, Acetylcholine receptor channel properties during development of Xenopus muscle cells in culture, J. Physiol. (Lond.) 357: 203–217.

    CAS  Google Scholar 

  • Brenner, H., and Sakmann, B., 1983, Neurotrophic control of channel properties at neuromuscular synapses of rat muscle, J. Physiol. (Lond.) 337: 159–171.

    CAS  Google Scholar 

  • Brett, R., Younkin, S., G. Knoieczkowski, and Slugg, R. M., 1982, Accelerated degradation of junctional acetylcholine receptor-alpha-bungarotoxin complexes in denervated rat diaphragm, Brain Res. 233: 133–142.

    PubMed  CAS  Google Scholar 

  • Buc-Caron, M.-H., Nystrom, P., and Fischbach, G. D., 1983, Induction of acetylcholine receptor synthesis and aggregation: Partial purification of low molecular weight activity, Dev. Biol. 95: 378–386.

    PubMed  CAS  Google Scholar 

  • Burden, S. J., 1977a, Development of the neuromusuclar junction in the chick embryo: The number, distribution, and stability of acetylcholine receptors, Dev. Biol. 57: 317–329.

    PubMed  CAS  Google Scholar 

  • Burden, S.]., 1977b, Acetylcholine receptors at the neuromuscular junction: Developmental change in receptor turnover, Dev. Biol. 61: 79–85.

    PubMed  Google Scholar 

  • Burden, S. J., 1982, Identification of an intracellular postsynaptic antigen at the frog neuromuscular junction, J. Cell Biol. 94: 521–530.

    PubMed  CAS  Google Scholar 

  • 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.

    Google Scholar 

  • Carson, S., Bon, S., Vigny, M., Massoulie, J., and Fardeau, M., 1979, Distribution of acetylcholinesterase molecular forms in neural and non-neural sections of human muscle, FEBS Lett. 97: 348–352.

    PubMed  CAS  Google Scholar 

  • Chow, I., 1980, Distribution of acetylcholine receptors in the myotomes of Xenopus laevis during normal development, Ph.D. thesis, McGill University, Montreal, Canada.

    Google Scholar 

  • Chow, I., and Cohen, M. W., 1983, Developmental changes in the distribution of acetylcholine receptors in the myotomes of Xenopus laevis, J. Physiol. (Lond.) 339: 553–571.

    CAS  Google Scholar 

  • Cisson, C. M., McQuarrie, C. H., Sketelj, J., McNamee, M. G., and Wilson, B. W., 1981, Molecular forms of acetylcholinesterase in chick embryonic fast muscle: Developmental changes and effects of DFP treatment, Dev. Neurosci. 4: 157.

    PubMed  CAS  Google Scholar 

  • Cohen, M. W., 1981, Development of an amphibian neuromuscular junction in vivo and in culture, J. Exp. Biol. 89: 43–56.

    CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Cohen, M. W., Greschner, M., and Tucci, M., 1984, In vivo development of cholinesterase at an amphibian neuromuscular junction in the absence of motor activity, J. Physiol. (Lond.) 348:57–66.

    CAS  Google Scholar 

  • Cohen, S. A., 1980, Early nerve-muscle synapses in vitro release transmitter over postsynaptic membrane having low acetylcholine sensitivity, Proc. Natl. Acad. Sci. USA 77: 644–648.

    PubMed  CAS  Google Scholar 

  • Cohen, S. A., and Fischbach, G. D., 1977, Clusters of acetylcholine receptors located at identified nerve-muscle synapses in vitro, Dev. Biol. 59: 24–38.

    PubMed  CAS  Google Scholar 

  • Cohen, S. A., and Pumplin, D. W., 1979, Clusters of intramembranous particles associated with binding sites for alpha-bungarotoxin in cultured chick myotubes, J. Cell Biol. 82: 494–516.

    PubMed  CAS  Google Scholar 

  • Couteaux, R., 1981, Structure of the subsynaptic sarcoplasm in the interfolds of the frog neuromuscular junction, J. Neurocytol. 10: 947–962.

    PubMed  CAS  Google Scholar 

  • Dennis, M. J., Ziskind-Conhaim, L., and Harris, A. J., 1981, Development of neuromuscular junctions in rat embryos, Dev. Biol. 81: 266–279.

    PubMed  CAS  Google Scholar 

  • Devreotes, P. N., and Fambrough, D. M., 1975, Acetylcholine receptor turnover in membranes of developing muscle fibers, J. Cell Biol. 65: 335–358.

    PubMed  CAS  Google Scholar 

  • Diamond, J., and Miledi, R., 1962, A study of fetal and new-born rat muscle fibers, J. Physiol. (Lond.) 162: 393–408.

    CAS  Google Scholar 

  • Dreyer, F., and Peper, K., 1974, The acetylcholine sensitivity of the neuromuscular junction of the frog, P/Jugers Arch. 398: 273–286.

    Google Scholar 

  • Dreyer, F., Peper, K., Akert, K., Sandri, C., and Moor, H., 1973, Ultrastructure of the “active zone” in the frog neuromuscular junction, Brain Res. 62: 373–380.

    PubMed  CAS  Google Scholar 

  • Ellisman, M. H., Rash, J. E., Staehlin, L. A., and Porter, K. R., 1976, Studies of excitable membranes. II. A comparison of specializations at neuromuscular junctions and non-junctional sarcolem- mac of mammalian fast and slow twitch muscle fibers, J. Cell Biol. 68: 752–774.

    PubMed  CAS  Google Scholar 

  • Fambrough, D. M., 1979, Control of acetylcholine receptors in skeletal muscle, Physiol. Rev. 59: 165–22 7.

    Google Scholar 

  • Fertuck, H. C., and Salpeter, M. M., 1974, Localization of acetylcholine receptors by 125I-alpha- bungarotoxin binding at mouse motor endplates, Proc. Natl. Acad. Sci. USA 71: 1376–1378.

    PubMed  CAS  Google Scholar 

  • Fertuck, H. C., and Salpeter, M. M., 1976, Quantitation of junctional and extrajunctional acetylcholine receptors by electron microscope autoradiography after 125I-alpha-bungarotoxin binding at mouse neuromuscular junctions, J. Cell Biol. 69: 144–158.

    PubMed  CAS  Google Scholar 

  • Filogama, G., and Gabella, G., 1967, The development of neuromuscular correlations in vertebrates, Arch. Biol. 78: 9–60.

    Google Scholar 

  • Fischbach, G. D., 1972, Synapse formation between dissociated nerve and muscle cells in low density cell cultures, Dev. Biol. 28: 407–429.

    PubMed  CAS  Google Scholar 

  • Fischbach, G. D., and Cohen, S. A., 1973, The distribution of acetylcholine sensitivity over unin- nervated and innervated muscle fibers grown in cell culture, Dev. Biol. 31: 147–162.

    PubMed  CAS  Google Scholar 

  • Fischbach, G. D., and Jessel, T. L., 1979, Induction of acetylcholine receptors and receptor cluster in embryonic myotubes, in: Ontogenesis and Functional Mechanisms of Peripheral Synapses, INSERM Symposium 13 ( J. Taxi, ed.), pp. 301–311, Elsevier/North-Holland, Amsterdam.

    Google Scholar 

  • Fischbach, G. D., and Schuetze, S. M., 1980, A post-natal decrease in acetylcholine channel open time at rat end-plates, J. Physiol. (Lond.) 303: 125–137.

    CAS  Google Scholar 

  • Fischbach, G. D., Fambrough, D., and Nelson, P. G., 1973, A discussion of neuron and muscle cell cultures, Fed. Proc. 32: 1636–1642.

    PubMed  CAS  Google Scholar 

  • Fischbach, G. D., Cohen, S. A., and Henkart, M. P., 1974, Some observations on trophic interaction between neurons and muscle fibers in cell culture, Ann. N.Y. Acad. Sci. 228: 35–46.

    PubMed  CAS  Google Scholar 

  • Fischbach, G. D., Frank, E., Jessel, T. M., Rubin, L. L., and Schuetze, S. M., 1979, Accumulation of acetylcholine receptors and cholinesterase at newly formed nerve-muscle synapses, Pharmacol. Rev. 30: 411–428.

    Google Scholar 

  • Frair, P., and Cohen, M. W., 1981, Degradation of acetylcholine receptors in innervated myotomes of Xenopus laevis maintained in organ culture, Neurosci. Abs. 7: 838.

    Google Scholar 

  • Frank, E., and Fischbach, G. D., 1979, Early events in neuromuscular junction formation in vitro. Induction of acetylcholine receptor clusters in the postsynaptic membrane and morphology of newly formed synapses, J. Cell Biol. 83: 143–158.

    PubMed  CAS  Google Scholar 

  • Giacobini, G., 1972, Embryonic and postnatal development of choline acetyltransferase activity in muscles and sciatic nerve of the chick, J. Neurochem. 19: 1401–1403.

    PubMed  CAS  Google Scholar 

  • Giacobini, G., Filogama, G., Weber, M., Boquet, P., and Changeux, J.-P., 1973, Effects of a snake alpha-neurotoxin on the development of innervated skeletal muscles in chick embryo, Proc. Natl. Acad. Sci. USA 70: 1708–1712.

    PubMed  CAS  Google Scholar 

  • Giacobini-Robecchi, M. G., Giacobini, G., Filogama, G., and Changeux, J.-P., 1975, Effects of the type A toxin from Clostridium botulinum on the development of skeletal muscles and their innervation in chick embryo, Brain Res. 83: 107–121.

    CAS  Google Scholar 

  • Gordon, T., Perry, R., Taffery, A. R., and Vrbova, G., 1974, Possible mechanisms determining synapse formation in developing skeletal muscle of the chick, Cell Tissue Res. 155: 13–25.

    PubMed  CAS  Google Scholar 

  • Guth, L., Zalewski, A. A., and Brown, W. C., 1966, Qualitative changes in cholinesterase activity of denervated soleplates following implantation of nerve into muscle, Exp. Neurol. 16: 136–147.

    PubMed  CAS  Google Scholar 

  • Hall, Z. W., 1973, Multiple forms of acetylcholinesterase and their distribution in endplate and non-endplate regions of rat diaphragm muscle, J. Neurobiol. 4: 343–361.

    PubMed  CAS  Google Scholar 

  • Hall, Z. W., and Kelly, R. B., 1971, Enzymatic detachment of endplate acetylcholinesterase form muscle, Nature New Biol. 232: 62–63.

    PubMed  CAS  Google Scholar 

  • Hamill, O. P., and Sakmann, B., 1981, Multiple conductance states of single acetylcholine receptor channels in embryonic muscle cells, Nature (Lond.) 294: 462–464.

    CAS  Google Scholar 

  • Harvey, A. L., and van Helden, D., 1981, Acetylcholine receptors in singly and multiply innervated skeletal muscle fibers of the chicken during development, J. Physiol. (Lond.) 317: 397–411.

    CAS  Google Scholar 

  • Heuser, J. E., Reese, T. S., and Landis, D. M. D., 1974, Functional changes in frog neuromuscular junctions studied with freeze-fracture, J. Neurocytol. 3: 109–131.

    PubMed  CAS  Google Scholar 

  • Hirano, H., 1967a, Ultrastructural study on the morphogenesis of the neuromuscular junction in the skeletal muscle of the chick, Z. Zellforsch. 79: 198–208.

    CAS  Google Scholar 

  • Hirano, H., 1967b, A histochemical study of the cholinesterase activity in the neuromuscular junction in developing chick skeletal muscles, Arch. Histol. Jpn. 28: 89–101.

    PubMed  CAS  Google Scholar 

  • Hooisma, J., Slaaf, D. W., Meeter, E., and Stevens, W. F., 1975, The innervation of chick striated muscle fibers by the chick ciliary ganglion in tissue culture, Brain Res. 85: 79–85.

    PubMed  CAS  Google Scholar 

  • Hourani, B. T., Tourain, B. F., Henkart, M. P., Carter, R. L., Marchesi, V. T., and Fischbach, G. D., 1974, Acetylcholine receptors of cultured muscle cells demonstrated with ferritin-alpha-bun- garotoxin conjugates, J. Cell Sci. 16: 473–479.

    PubMed  CAS  Google Scholar 

  • Hume, R. I., Role, L. W., and Fischbach, G. D., 1983, Acetylcholine release from growth cones detected with patches of acetylcholine receptor rich membranes, Nature (Lond.) 305: 632–633.

    CAS  Google Scholar 

  • Inestrosa, N., Ziskind-Conhaim, L., and Hall, Z. W., 1984, Acetylcholinesterase in developing muscle fibers, in: Neuromuscular Diseases ( G. Serratrice, D. Cros, C. Desnuelle, J.-L. Gastaut, J.- F. Pellisier, J. Pouget, and A. Schiano, eds.), pp. 437–441, Raven Press, New York.

    Google Scholar 

  • Jacob, M., and Lentz, T. L., 1979, Localization of acetylcholine receptor by means of horseradish peroxidase-alpha-bungarotoxin during formation and development of the neuromuscular junction in the chick embryo, J. Cell Biol. 82: 195–211.

    PubMed  CAS  Google Scholar 

  • Jessel, 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.

    Google Scholar 

  • Jones, R., and Vrbova, G., 1974, Two factors responsible for the development of denervation hypersensitivity, J. Physiol. (Lond.) 236: 517–538.

    CAS  Google Scholar 

  • Jones, R., and Vyskocil, F., 1975, An electrophysiological examination of the changes in skeletal muscle fibers in response to degenerating nerve tissue, Brain Res. 88: 309–317.

    PubMed  CAS  Google Scholar 

  • Juntunen, J., 1974, Induction of the postsynaptic membrane, Med. Biol. 52: 164–169.

    PubMed  CAS  Google Scholar 

  • Kano, M., and Shimada, Y., 1971, Innervation and acetylcholine sensitivity of skeletal muscle cells differentiated in vitro from chick embryo, J. Cell Physiol. 78: 233–248.

    PubMed  CAS  Google Scholar 

  • Kao, I., and Drachman, D. B., 1977, Myasthenic immunoglobulin accelerates acetylcholine receptor degradation, Science 196; 527–529.

    PubMed  CAS  Google Scholar 

  • Karnovsky, M. J., 1964, The localization of cholinesterase activity in rat cardiac muscle by electron microscopy,J.Cell Biol. 23: 217–232.

    PubMed  CAS  Google Scholar 

  • Kato, A. C., Vrachliotis, A., Fulpius, B., and Dunant, Y., 1980, Molecular forms of acetylcholinesterase in chick muscle and ciliary ganglion: Embryonic tissues and cultured cells, Dev. Biol. 76: 222–228.

    PubMed  CAS  Google Scholar 

  • Katz, B., 1966, Nerve, Muscle, and Synapse, McGraw-Hill, New York.

    Google Scholar 

  • Katz, B., and Miledi, R., 1972, The statistical nature of the acetylcholine potential and its molecular components, J. Physiol. (Lond.) 224: 665–699.

    CAS  Google Scholar 

  • Katz, B., and Miledi, R., 1973, The binding of ACh to receptors and its removal from the synaptic cleft,J.Physiol. (Lond.) 231: 549–574.

    CAS  Google Scholar 

  • Kelly, A. M., and Zacks, S. I., 1969, The fine structure of motor endplate morphogenesis, J. Cell Biol. 42: 154–169.

    PubMed  CAS  Google Scholar 

  • Kidokoro, Y., 1980, Developmental changes of spontaneous synaptic potential properties in the rat neuromuscular contact formed in culture, Dev. Biol. 78: 231–241.

    PubMed  CAS  Google Scholar 

  • Kidokoro, Y., and Patrick, J., 1978, Correlation between miniature endplate potential amplitudes and acetylcholine receptor densities in the neuromuscular contact formed in vitro, Brain Res. 142: 368–373.

    PubMed  CAS  Google Scholar 

  • Kidokoro, Y., and Yeh, E., 1982, Initial synaptic transmission at the growth cone in Xenopus nerve-muscle cultures, Proc. Natl. Acad. Sci. USA 79: 6727–6731.

    PubMed  CAS  Google Scholar 

  • Kidokoro, Y., Anderson, M. J., and Gruener, R., 1980, Changes in synaptic potential properties during acetylcholine receptor accumulation and neurospecific interactions in Xenopus nerve- muscle cell culture, Dev. Biol. 78: 464–485.

    PubMed  CAS  Google Scholar 

  • Klymkowsky, M. W., Lappin, R. I., and Rubin, L. L., 1983, Biosynthesis and extracellular transport of acetylcholinesterase in primary muscle cultures, Neurosci. Abs. 13(1): 344.

    Google Scholar 

  • Koenig, J., and Rieger, F., 1981, Biochemical stability of the acetylcholinesterase molecular forms after cytochemical staining: Postnatal focalization of 16S acetylcholinesterase in rat muscle, Dev. Neurosci. 4: 249–257.

    PubMed  CAS  Google Scholar 

  • Koenig, J., Bournaud, R., and Rieger, F., 1979, Acetylcholinesterase and formation in striated muscle, in: Ontogenesis and Functional Mechanisms of Peripheral Synapses ( J. Taxi, ed.), pp. 313–326, Elsevier/North-Holland, Amsterdam.

    Google Scholar 

  • Koenig, J., deLaporte, S., Massoulie, J., and Vigny, M., 1984, Regulation of the acetylcholinesterase molecular forms in nerve-muscle cell cultures, in: Neuromuscular Diseases ( G. Serratrice, D. Cros, C. Desnuelle, J.-L. Gastaut, J.-F. Pellisier, J. Pouget, and A. Schiano, eds.), pp. 443–446, Raven Press, New York.

    Google Scholar 

  • Korneliussen, H., and Jansen, J. K. S., 1976, Morphological aspects of the elimination of poly- neuronal innervation of skeletal muscle fibers in newborn rats, ]. Neurocytol. 5: 591–604.

    PubMed  CAS  Google Scholar 

  • Kuffler, S. W., and Yoshikami, D., 1975, The distribution of acetylcholine sensitivity at the postsynaptic membrane of vertebrate skeletal twitch muscles: Iontophoretic mapping in the micron range, J. Physiol. (Lond.) 244: 703–730.

    CAS  Google Scholar 

  • Kullberg, R. W., Lentz, T. L., and Cohen, M. W., 1977, Development of the myotomal neuromuscular junction in Xenopus laevis: An electrophysiological and fine-structural study, Dev. Biol. 60:101–120.

    PubMed  CAS  Google Scholar 

  • Kullberg, R. W., Mickelberg, F. S., and Cohen, M. W., 1980, Contribution of cholinesterase to development decreases in the time course of synaptic potentials at an amphibian neuromuscular junction, Dev. Biol. 75: 255–267.

    PubMed  CAS  Google Scholar 

  • Kullberg, R. W., Brehm, P., and Steinbach, J. H., 1981, Nonjunctional acetylcholine receptor channel open time decreases during development of Xenopus muscle, Nature (Lond.) 289: 411–413.

    CAS  Google Scholar 

  • Landmesser, L., and Morris, D. G., 1975, The development of functional innervation in the hindlimb of the chick embryo, J. Physiol. (Lond.) 249: 301–326.

    CAS  Google Scholar 

  • Lomo, T., and Slater, C. R., 1980, Control of junctional acetylcholinesterase by neural and muscular influence in the rat, J. Physiol. (Lond.) 303: 191–202.

    CAS  Google Scholar 

  • Loring, R. H., and Salpeter, M. M., 1980, Denervation increases turnover rate of junctional acetylcholine receptors, Proc. Natl. Acad. Sci. USA 77: 2293–2297.

    PubMed  CAS  Google Scholar 

  • MacKay, B., Muir, A. R., and Peters, A., 1960, Observations on the terminal innervation of segmental muscle fibers in amphibia, Acta Anat. 40: 1–12.

    PubMed  CAS  Google Scholar 

  • Markelonis, G. J., Oh, T. H., Eldefrawi, M. E., and Guth, L., 1982, Sciatin: A myotrophic protein increases the number of acetylcholine receptors and receptor clusters in cultured skeletal muscle, Dev. Biol. 89: 353–361.

    PubMed  CAS  Google Scholar 

  • Marshall, L. M., Sanes, J. R., and McMahan, U. J., 1977, Reinnervation of original synaptic sites on muscle fiber basement after disruption of the muscle cells, Proc. Natl. Acad. Sci. USA 74: 3073–3077.

    PubMed  CAS  Google Scholar 

  • Massoulie, J., and Bon, S., 1982, The molecular forms of cholinesterase and acetylcholinesterase in vertebrates, Annu. Rev. Neurosci. 5: 57–106.

    CAS  Google Scholar 

  • Matthews-Bellinger, J., and Salpeter, M., 1978, Distribution of acetylcholine receptors at frog neuromuscular junctions with a discussion of some physiological implications, ]. Physiol. (Lond.) 279: 197–213.

    CAS  Google Scholar 

  • McMahan, U. J., Sanes, J. R., and Marshall, L. M., 1978, Cholinesterase is associated with the basal lamina at the neuromuscular junction, Nature (Lond.) 271: 172–174.

    CAS  Google Scholar 

  • McMahan, U. J., Sargent, P. P., Rubin, L. L., and Burden, B.]., 1979, Factors that influence the organization of acetylcholine receptors in regenerating muscle are associated with the basal lamina at the neuromuscular junction, in: Ontogenesis and Functional Mechanisms of Peripheral Synapses ( J. Taxi, ed.), pp. 345–354, Elsevier/North-Holland, Amsterdam.

    Google Scholar 

  • Michler, A., and Sakmann, B., 1980, Receptor stability and channel conversion in the subsynaptic membrane of the developing mammalian neuromuscular junction, Dev. Biol. 80: 1–17.

    PubMed  CAS  Google Scholar 

  • Miledi, R., 1960, Junctional and extrajunctional acetylcholine receptors in skeletal muscle fibers, J. Physiol. (Lond.) 151: 24–30.

    CAS  Google Scholar 

  • Moody-Corbett, F., and Cohen, M. W., 1981, Localization of cholinesterase at sites of high acetylcholine receptor density on embryonic amphibian muscle cells cultured without nerve, J. Neurosci. 1: 596–605.

    PubMed  CAS  Google Scholar 

  • Moody-Corbett, F., and Cohen, M. W., 1982a, Influence of nerve on the formation and survival of acetylcholine receptor and cholinesterase patches on embryonic Xenopus muscle cells in culture, J. Neurosci. 2: 633–646.

    PubMed  CAS  Google Scholar 

  • Moody-Corbett, F., and Cohen, M. W., 1982b, Increased adhesiveness at sites of high acetylcholine receptor density on embryonic amphibian muscle cells cultured without nerve, J. Embryol. Exp. Morphol. 72: 53–69.

    PubMed  CAS  Google Scholar 

  • Moody-Corbett, F., Weldon, P. R., and Cohen, M. W., 1982, Cholinesterase localization at sites of nerve contact on embryonic amphibian muscle cells in culture, J. Neurocytol. 11: 381–394.

    PubMed  CAS  Google Scholar 

  • Moody-Corbett, F., Brehm, P., and Kullberg, R. W., 1983, Functional properties of non-junctional acetylcholine receptors on developing muscle, Can. Fed. Biol. Soc. PA236.

    Google Scholar 

  • Nakajima, Y., Kidokoro, Y., and Klier, F. G., 1980, Development of functional neuromuscular junctions in vitro: An ultra-structural and physiological study, Dev. Biol. 77: 52–72.

    PubMed  CAS  Google Scholar 

  • Nicolet, M., and Reiger, F., 1981, Formes moléculaires de l’acetylcholinesterase du muscle squelet- tique de Grenouille: Effets de l’enervation, C.R. Soc. Biol. 175: 316–322.

    CAS  Google Scholar 

  • Nieuwkoop, P. D., and Faber,]., 1967, Normal Table of Xenopus laevis (Daudin), 2nd éd., North- Holland, Amsterdam.

    Google Scholar 

  • Obata, K., 1977, Development of neuromuscular transmission in culture with a variety of neurons and in the presence of cholinergic substances and tetrodotoxin, Brain Res. 119: 141–153.

    PubMed  CAS  Google Scholar 

  • Oh, T. H., and Markelonis, G. J., 1982, Chicken serum transferrin duplicates the myotrophic effects of sciatin on cultured muscle cells, J. Neurosci. Res. 8: 535–545.

    PubMed  CAS  Google Scholar 

  • Oppenheim, R. W., Pittman, R., Gray, M., and Maderdrut, J. L., 1978, Embryonic behavior, hatching and neuromuscular development in the chick following a transient reduction of spontaneous motility and sensory input by neuromuscular blocking agents, J. Comp. Neurol. 179: 619–640.

    PubMed  CAS  Google Scholar 

  • Peng, B., and Nakajima, Y., 1978, Membrane particle aggregates in innervated and non-innervated cultures of Xenopus embryonic muscle cells, Proc. Natl. Acad. Sci. USA 75: 500–504.

    PubMed  CAS  Google Scholar 

  • Peng, B., Bridgman, P. C., Nakajima, S., Greenberg, A., and Nakajima, Y., 1979, A fast development of presynaptic function and structure of the neuromusucular junction in Xenopus tissue culture, Brain Res. 167: 379–384.

    PubMed  CAS  Google Scholar 

  • Peng, B., Nakajima, Y., and Bridgman, P. C., 1980, Development of the post-synaptic membrane in Xenopus neuromuscular cultures observed by freeze-fracture and thin-section electron microscopy, Brain Res. 196: 11–31.

    PubMed  CAS  Google Scholar 

  • Peng, B., Cheng, P.-C., and Luther, P. W., 1981, Formation of ACh receptor clusters induced by positively charged latex beads, Nature (Lond.) 292: 831–834.

    CAS  Google Scholar 

  • Peper, K., and McMahan, U. J., 1972, Distribution of acetylcholine receptors in the vicinity of nerve terminals on skeletal muscle of the frog, Proc. R. Soc. Lond. B. 181: 431–440.

    CAS  Google Scholar 

  • Popiella, H., Beach, R. L., and Festoff, B. W., 1984, Developmental appearance of acetylcholinesterase molecular forms in cultured primary chick muscle cells, in: Neuromuscular Diseases ( G. Serratrice, D. Cros, C. Desnuelle, J.-L. Gastaut, J.-F. Pellisier, J. Pouget, and A. Schiano, eds.), pp. 447–450, Raven Press, New York.

    Google Scholar 

  • Porter, C. W., and Barnard, E. A., 1975, The density of cholinergic receptors at the endplate postsynaptic membrane: Ultrastructural studies in two mammalian species, J. Membrane Biol. 20: 31–49.

    CAS  Google Scholar 

  • Pumplin, D. W., and Fambrough, D. M., 1982, Turnover of acetylcholine receptors in skeletal muscle, Annu. Rev. Physiol. 44: 319–335.

    PubMed  CAS  Google Scholar 

  • Rash, J. E., and Ellisman, M. H., 1974, Studies of excitable membranes. I. Macromolecular specializations of the neuromuscular junction and the nonjunctional sarcolemma, J. Cell Biol. 63: 567–586.

    PubMed  CAS  Google Scholar 

  • Reiger, F., Koenig, J., and Vigny, M., 1980, Spontaneous contractile activity and the presence of the 16S form of acetylcholinesterase in rat muscle cells in culture: Reversible suppressive action of tetrodotoxin, Dev. Biol. 76: 358–365.

    Google Scholar 

  • Reiness, C. G., and Weinberg, C. B., 1981, Metabolic stabilization of acetylcholine receptors at newly formed neuromuscular junction in rat, Dev. Biol. 84: 247–254.

    PubMed  CAS  Google Scholar 

  • Ripley, K. L., and Provine, R. R., 1972, Neural correlates of embryonic motility in the chick, Brain Res. 45: 127–134.

    PubMed  CAS  Google Scholar 

  • Rotundo, R. L., and Fambrough, D. M., 1979, Molecular forms of chicken embryo acetylcholinesterase in vitro and in vivo, J. Biol. Chem. 254: 4790–4799.

    PubMed  CAS  Google Scholar 

  • Rubin, L. L., Schuetze, S. M., and Fischbach, G. D., 1979, Accumulation of acetylcholinesterase at newly formed nerve-muscle synapses, Dev. Biol. 69: 46–58.

    PubMed  CAS  Google Scholar 

  • Rubin, L. L., Schuetze, S. M., Weill, C. L., and Fischbach, G. D., 1980, Regulation of acetylcholinesterase appearance at neuromuscular junctions in vitro, Nature (Lond.) 283: 264–267.

    CAS  Google Scholar 

  • Salpeter, M. M., Spanton, S., Holley, K., and Podleski, T. R., 1982, Brain extract causes acetylcholine receptor redistribution which mimics some early events at developing neuromuscular junctions,J.Cell Biol. 93: 417–425.

    PubMed  CAS  Google Scholar 

  • Sanes, J. R., 1983, Roles of extracellular matrix in neural development, Annu. Rev. Physiol. 45:581– 600.

    Google Scholar 

  • Sanes, J. R., and Hall, Z. W., 1979, Antibodies that bind specifically to synaptic sites on muscle fiber basal lamina, J. Cell Biol. 83: 357–370.

    PubMed  CAS  Google Scholar 

  • Sanes, J. R., and Lawrence, J. C., 1983, Activity-dependent accumulation of basal lamina by cultured rat myotubes, Dev. Biol. 97: 123–136.

    PubMed  CAS  Google Scholar 

  • Sanes, J. R., Marshall, L. M., and McMahan, U. J., 1978, Reinnervation of muscle fiber basal lamina after removal of myofibers, J. Cell Biol. 78: 176–198.

    PubMed  CAS  Google Scholar 

  • Schaffner, A. E., and Daniels, M. P., 1982, Conditioned medium from cultures of embryonic neurons contains a high molecular weight factor which induces acetylcholine receptor aggregation on cultured myotubes, J. Neurosci. 2: 623–632.

    PubMed  CAS  Google Scholar 

  • Schuetze, S. M., 1980, The acetylcholine channel open time in chick muscle is not decreased following innervation, ]. Physiol. (Lond.) 303: 111–124.

    CAS  Google Scholar 

  • Schuetze, S. M., and Vicini, S., 1983, Denervation blocks the normal postnatal decrease in rat endplate channel open time, Neurosci. Ahs. 9: 1108.

    Google Scholar 

  • Schuetze, S. M., Frank, E., and Fischbach, G. D., 1978, Channel open time and metabolic stability of synaptic and extrasynaptic acetylcholine receptors on cultured chick myotubes, Proc. Natl. Acad. Sci. USA 75: 520–523.

    PubMed  CAS  Google Scholar 

  • Sisto-Daneo, L., and Filogama, G., 1975, Differentiation of synaptic area in “slow” and “fast” muscle fibers, ]. Submicrosc. Cytol. 7: 121–131.

    Google Scholar 

  • Sketelj, J., and Brzin, M., 1980, 16S acetylcholinesterase in endplate-free regions of developing rat diaphragm, Neurochem. Res. 5: 653–658.

    Google Scholar 

  • Stanley, E. F., and Drachman, B., 1983, Rapid degradation of “new” acetylcholine receptors at neuromuscular junction, Science 222: 67–69.

    PubMed  CAS  Google Scholar 

  • Steinbach, J. H., 1981, Developmental changes in acetylcholine receptor aggregates at rat skeletal neuromuscular junctions, Dev. Biol. 84: 267–276.

    PubMed  CAS  Google Scholar 

  • Steinbach,. J. H., Merlie, J., Heinemann, S., and Bloch, R., 1979, Degradation of junctional and extrajunctional acetylcholine receptors by developing rat skeletal muscle, Proc. Natl. Acad. Sci. USA 76: 3547–3551.

    Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Teravainen, H., 1968, Development of the myoneural junction in the rat, Z. Zellerforsch. 87:249– 265.

    Google Scholar 

  • Vigny, M., and Koenig, J., 1978, Neural induction of the 16S acetylcholinesterase in muscle cell culture, Nature (Lond.) 271: 75–77.

    Google Scholar 

  • Vigny, M., Koenig, J., and Reiger, F., 1976, The motor end-plate specific form of acetylcholinesterase: Appearance during embryogenesis and reinnervation of rat muscle, J. Neurochem. 27: 1347–1353.

    PubMed  CAS  Google Scholar 

Download references

Author information

Author notes

  1. Frances Moody-Corbett (Faculty of Medicine)

    Present address: Division of Basic Medical Sciences, Memorial University of Newfoundland, St John’s, Newfoundland, A1B 3V6, Canada

Authors and Affiliations

  1. Department of Physiology, Tuffs University School of Medicine, Boston, Massachusetts, 02111, USA

    Frances Moody-Corbett (Faculty of Medicine)

Authors
  1. Frances Moody-Corbett
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. University of Calgary, Calgary, Alberta, Canada

    Leon W. Browder

Rights and permissions

Reprints and permissions

Copyright information

© 1986 Plenum Press, New York

About this chapter

Cite this chapter

Moody-Corbett, F. (1986). Formation of the Vertebrate Neuromuscular Junction. In: Browder, L.W. (eds) The Cellular Basis of Morphogenesis. Developmental Biology, vol 2. Springer, Boston, MA. https://doi.org/10.1007/978-1-4613-2141-5_16

Download citation

  • DOI: https://doi.org/10.1007/978-1-4613-2141-5_16

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-1-4612-9264-7

  • Online ISBN: 978-1-4613-2141-5

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics

Search

Navigation