Advertisement

Cell and Tissue Research

, Volume 168, Issue 1, pp 101–115 | Cite as

Microtubule-synaptic vesicle associations in cultured rat spinal cord neurons

  • Margaret M. Bird
Article

Summary

This paper describes new ultrastructural features of neural processes and of synapses in cultured CNS tissue treated with albumin before fixation using a modification of the technique recently introduced by Gray (1975). Nerve fibre bundles in explants of foetal spinal cord grown in vitro for 15–18 days were transected microsurgically. After transection the cultures were exposed to 20% albumin in distilled water and then fixed in unbuffered osmium tetroxide followed by unbuffered glutaraldehyde.

In this material, but not in controls (injured but not exposed to albumin; exposed to albumin without injury) microtubules were found within many axonal varicosities, often situated close to presynaptic membrane specializations. These microtubules were closely associated with vesicles resembling synaptic vesicles, which were occasionally aligned in rows along the microtubules. Similar vesicle-microtubule associations were also found in non-terminal axons. Microtubules were also observed very close to some postsynaptic densities.

The possibility that the microtubule-vesicle associations are involved in vesicle movements (along axons and/or within axon terminals) is discussed. A more direct involvement of microtubules in terminals in the mechanism of transmitter release is also considered.

Key words

Synapses Microtubules Albumin Tissue culture 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Banker, G., Churchill, L., Cotman, C.W.: Proteins of the postsynaptic density. J. Cell Biol. 63, 456–465 (1974)Google Scholar
  2. Bird, M.M., James, D.W.: The development of synapses in vitro between previously dissociated chick spinal cord neurons. Z. Zellforsch. 140, 203–216 (1973)Google Scholar
  3. Behnke, O.: An outer component of microtubules. Nature (Lond.) 257, 709–710 (1975)Google Scholar
  4. Breemen, V.L. van, Andersen, E., Reger, J.F.: An attempt to determine the origin of synaptic vesicles. Exp. Cell Res., Suppl. 5, 153–167 (1958)Google Scholar
  5. Ceccarelli, B., Hurlbut, W.P., Mauro, A.: Depletion of vesicles from frog neuromuscular junctions by prolonged tetanic stimulation. J. Cell Biol. 54, 30–38 (1972)Google Scholar
  6. Grainger, A.F., James, D.W.: Mitochondrial extensions associated with microtubules in outgrowing processes from chick spinal cord in vitro. J. Cell Sci. 4, 729–737 (1969)Google Scholar
  7. Gray, E.G.: Pre-synaptic microtubules and their associations with synaptic vesicles. Proc. roy. Soc. B 190, 369–372 (1975)Google Scholar
  8. Gray, E.G.: Microtubules in synapses of the retina. J. Neurocytol. 5 (in press) (1976)Google Scholar
  9. Heuser, J.E., Reese, T.S.: Evidence for recycling of synaptic vesicle membrane during transmitter release at the frog neuromuscular junction. J. Cell Biol. 57, 315–344 (1973)Google Scholar
  10. Jacobs, M., Bennett, P.M., Dickens, M.J.: Duplex microtubule is a new form of Tubulin assembly induced by polycations. Nature (Lond.) 257, 709–710 (1975)Google Scholar
  11. Kanaseki, T., Kadota, E.: The vesicle in a basket. J. Cell Biol. 42, 202–220 (1969)Google Scholar
  12. Lieberman, A.R.: Microtubule-associated smooth endoplasmic reticulum in the frog's brain. Z. Zellforsch. 116, 564–574 (1971)Google Scholar
  13. Malaisse, W.J., Malaisse-Lagae, F., Van Obberghen, E., Somers, G., Devis, G., Ravazzola, M., Orci, L.: Rôle of microtubules in the phasic pattern of insulin release. Ann. N.Y. Acad. Sci. 253, 630–652 (1975)Google Scholar
  14. Matus, A.I., Walters, B.B., Mughal, S.: Immunohistochemical demonstration of Tubulin associated with microtubules and synaptic junctions in mammalian brain. J. Neurocytol. 4, 733–744 (1975)Google Scholar
  15. Model, P.G., Highstein, A.M., Bennett, M.V.L.: Depletion of vesicles and fatigue of transmission at a vertebrate synapse. Brain Res. 98, 209–228 (1975)Google Scholar
  16. Poisner, A.M., Cooke, P.: Microtubules and the adrenal medulla. Ann. N.Y. Acad. Sci. 253, 653–669 (1975)Google Scholar
  17. Pysh, J.J., Wiley, R.G.: Synaptic depletion and recovery in cat sympathetic ganglia electrically stimulated in vivo. J. Cell Biol. 60, 365–374 (1974)Google Scholar
  18. Schmitt, P.O.: The molecular biology of neuronal fibrous protein. Neurosci. Res. Prog. Bull. 6, 119–144 (1968)Google Scholar
  19. Smith, D.S., Järlfors, U., Béranek, R.: The organisation of synaptic axoplasm in the lamprey (Petromyzon marinus) central nervous tissue. J. Cell Biol. 46, 199–219 (1970)Google Scholar
  20. Smith, D.S., Järlfors, U., Cameron, B.F.: Morphological evidence for the participation of microtubules in axonal transport. Ann. N.Y. Acad. Sci. 253, 472–506 (1975)Google Scholar
  21. Sorimachi, M.F., Oesch, F., Thoenen, H.: Effect of colchicine and cytochalasin-B on the release of 3H-norephinephrine from guinea pig atria evoked by high potassium, nicotine, and tyramine. Naunyn-Schmiedebergs Arch. exp. Path. Pharmak. 276, 1–12 (1975)Google Scholar
  22. Westrum, L.E., Gray, E.G.: Microtubules and membrane specializations. Brain Res., in press (1976)Google Scholar
  23. Wooton, G.F., Kopin, I.J., Axelrod, J.: Effects of colchicine and vinblastine on axonal transport and transmitter release in sympathetic nerves. Ann. N.Y. Acad. Sci. 253, 528–534 (1975)Google Scholar

Copyright information

© Springer-Verlag 1976

Authors and Affiliations

  • Margaret M. Bird
    • 1
  1. 1.Department of AnatomyUniversity College LondonEngland

Personalised recommendations