Journal of Neurocytology

, Volume 12, Issue 4, pp 661–671 | Cite as

Differentiation of motor nerve terminals formed in the absence of muscle fibres

  • Marcie A. Glicksman
  • Joshua R. Sanes
Article
Received:
Accepted:

Summary

During reinnervation of frog skeletal muscle, axons form functional nerve terminals at original synaptic sites on denervated myofibres. When muscle is damaged as well as denervated, myofibres decompose but their sheaths of basal lamina (BL) survive. Despite the absence of myofibres, axons regenerate to contact BL and there acquire clusters of synaptic vesicles and membrane-associated dense patches that resemble active zones; BL regulates this differentiation. We show here that these BL-associated axonal segments appear smaller and contain fewer active zones than terminals on intact myofibres in the same preparation. However, terminals formed on BL sheaths are capable of activity-dependent recycling of synaptic vesicles (demonstrated by tracer uptake), and bear an antigen normally present in terminals but not preterminal axons (demonstrated by immunofluorescence). Thus, axons can acquire functional and biochemical, as well as morphological, characteristics of normal motor nerve terminals in the absence of a postsynaptic cell.

Keywords

Skeletal Muscle Muscle Fibre Synaptic Vesicle Nerve Terminal Basal Lamina 
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.
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References

  1. Carlson, S. S. &Kelly, R. B. (1980) An antiserum specific for cholinergic synaptic vesicles from electric organ.Journal of Cell Biology 87, 98–103.Google Scholar
  2. Ceccarelli, B. &Hurlbut, W. P. (1975) The effects of prolonged repetitive stimulation in hemicholinium on the frog neuromuscular junction.Journal of Physiology 247, 163–88.Google Scholar
  3. Ceccarelli, B. &Hurlbut, W. P. (1980) Vesicle hypothesis of the release of quanta of acetylcholine.Physiological Reviews 60, 396–441.Google Scholar
  4. Ceccarelli, B., Hurlbut, W. P. &Mauro, A. (1972) Depletion of vesicles from frog neuromuscular junctions by prolonged tetanic stimulation.Journal of Cell Biology 54, 30–8.Google Scholar
  5. Ding, R. (1982) Lack of correlation between physiological and morphological features of regenerating frog neuromuscular junctions.Brain Research 253, 47–55.Google Scholar
  6. Glicksman, M. &Sanes, J. R. (1982) Functional and biochemical differentiation of motor nerve terminals formed in the absence of muscle fibers.Neuroscience Abstracts 8, 128.Google Scholar
  7. Graham Jr, R. C. &Karnovsky, M. J. (1966) The early stages of absorption of injected horseradish peroxidase in the proximal tubules of mouse kidney: ultrastructural cytochemistry by a new technique.Journal of Histochemistry and Cytochemistry 14, 291–302.Google Scholar
  8. Heuser, J. E. &Reese, T. S. (1973) Evidence for recycling of synaptic vesicle membrane during transmitter release at the frog neuromuscular junction.Journal of Cell Biology 57, 315–44.Google Scholar
  9. Holtzman, E. (1977) The origin and fate of secretory packages, especially synaptic vesicles.Neuroscience 2, 327–55.Google Scholar
  10. Holtzman, E., Freeman, A. R. &Kashner, L. A. (1971) Stimulation-dependent alterations in peroxidase uptake at lobster neuromuscular junctions.Science 173, 733–6.Google Scholar
  11. Karnovsky, M. J. (1964) The localization of cholinesterase activity in rat cardiac muscle by electron microscopy.Journal of Cell Biology 23, 217–32.Google Scholar
  12. McMahan, U. J., Edgington, D. R. &Kuffler, D. P. (1980) Factors that influence regeneration of the neuromuscular junction.Journal of Experimental Biology 89, 31–42.Google Scholar
  13. McMahan, U. J., Sanes, J. R. &Marshall, L. M. (1978) Cholinesterase is associated with the basal lamina at the neuromuscular junction.Nature 271, 172–4.Google Scholar
  14. Nakajima, Y., Kidokoro, Y. &Klier, F. G. (1980) The development of functional neuromuscular junctionsin vitro: an ultrastructural and physiological study.Developmental Biology 77, 52–72.Google Scholar
  15. Rees, R. P. (1978) The morphology of interneuronal synaptogenesis: a review.Federation Proceedings 37, 2000–9.Google Scholar
  16. Sanes, J. R. (1983) Roles of extracellular matrix in neural development.Annual Reviews of Physiology 45, 581–600.Google Scholar
  17. Sanes, J. R., Carlson, S. S., Von Wedel, R. &Kelly, R. B. (1979) Antiserum specific for nerve terminals in skeletal muscle.Nature 280, 403–4.Google Scholar
  18. Sanes, J. R. &Cheney, J. M. (1982) Lectin binding reveals a synapse-specific carbohydrate in skeletal muscle.Nature 300, 646–7.Google Scholar
  19. Sanes, J. R. &Hall, Z. W. (1979) Antibodies that bind specifically to synaptic sites on muscle fiber basal lamina.Journal of Cell Biology 83, 357–70.Google Scholar
  20. Sanes, J. R. &Lawrence Jr, J. C. (1983) Activity-dependent accumulation of basal lamina by cultured rat myotubes.Developmental Biology in press.Google Scholar
  21. Sanes, J. R., Marshall, L. M. &McMahan, U. J. (1978) Reinnervation of muscle fiber basal lamina after removal of myofibers. Differentiation of regenerating axons at original synaptic sites.Journal of Cell Biology 78, 176–98.Google Scholar
  22. Silberstein, L. Inestrosa, N. &Hall, Z. W. (1982) Aneural muscle cell cultures make synaptic basal lamina components.Nature 294, 143–5.Google Scholar
  23. Von Wedel, R. J., Carlson, S. S. &Kelly, R. B. (1981) Transfer of synaptic vesicle antigens to the presynaptic plasma membrane during exocytosis.Proceedings of the National Academy of Sciences USA 78, 1014–8.Google Scholar

Copyright information

© Chapman and Hall Ltd 1983

Authors and Affiliations

  • Marcie A. Glicksman
    • 1
  • Joshua R. Sanes
    • 1
  1. 1.Department of Physiology and BiophysicsWashington University School of MedicineSt LouisUSA

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