Summary
The axonal transport of 3H-fucose labelled glycoproteins along the developing optic pathway was studied by radioautography in 7-day and 18-day chick embryos after injection of 3H-fucose into the right eye.
In the 7-day embryos an axonal transport of labelled glycoproteins could be traced towards axon tops in the anteromedial aspect of the left optic lobe. The glycoprotein radioactivity reached the distal parts of the growing optic axons between 2 and 4 h after intraocular injection of labelled precursor indicating a rapid axonal transport of the order of at least 20 to 50 mm day-1.
In the 18-day embryos fucose labelled glycoproteins reached the optic tectum at 2 h after 3H-fucose injection. When the fate of the glycoproteins was analyzed at later survival times an accumulation of radioactivity in the tectal layers containing synapses of optic origin could be found for at least 48 h after precursor injection in the 18-day embryos. The present data indicate that throughout development glycoproteins synthesized in the nerve cell bodies reach the distal parts of growing and maturing axons. The hypothesis is proposed that glycoproteins rapidly reach the preterminal portion of the optic axons where they become integral proteins of the axolemma. From this location they may flow within the membrane structure to reach the synapse.
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Bennett, G., Di Giamberadino, L., Koenig, H.L., Droz, B.: Axonal migration of protein and glycoprotein to nerve endings. II. Radioautographic analysis of the renewal of glycoproteins in nerve endings of chicken ciliary ganglion after intracerebral injection of 3H-fucose and 3H-glucosamine. Brain Res. 60, 129–146 (1973)
Bennett, H. S.: Morphological aspects of extracellular polysaccharides. J. Histochem. Cytochem. 11, 14–23 (1963)
Bocci, V., Winzler, R. J.: Metabolism of L-fucose-14C and of fucose glycoproteins in the rat. Amer. J. Physiol. 216, 1337–1342 (1969)
Cowan, W.M.: Studies on the development of the avian visual system. In: D.G. Pease (ed.), Cellular aspects of neural growth and differentiation, p. 177–222, Berkeley: UCLA University Press 1971
Cowan, W.M., Adamson, L., Powell, T.P. S.: An experimental study of the avian visual system. J. Anat. (Lond.) 95, 54–562 (1961)
Cowan, W.M., Gottlieb, D.I., Hendrickson, A., Price, J.L., Woolsey, T. A.: The autoradiographic demonstration of axonal connections in the central nervous system. Brain Res. 37, 21–51 (1972)
Crossland, W. J., Cowan, W.M., Kelly, J.P.: Observations on the transport of radioactively labeled proteins in the visual system of the chick. Brain Res. 56, 77–105 (1973)
Droz, B., Koenig, H.L., Di Giamberardino, L.: Axonal migration of protein and glycoprotein to nerve endings. I Radioautographic analysis of the renewal of protein and glycoprotein in nerve endings of chicken ciliary ganglion after intracerebral injection of 3H-lysine. Brain Res. 60, 93–127 (1973)
Edström, A., Mattson, H.: Rapid axonal transport in vitro in the sciatic system of the frog of fucose-, glucosamine-, and sulphate-containing material. J. Neurochem. 19, 1771–1729 (1972)
Forman, D. S., Grafstein, B., McEwen, B. S.: Rapid axonal transport of 3H-fucosyl glycoproteins in the goldfish optic system. Brain Res. 48, 307–342 (1972)
Hamburger, V., Hamilton, H.L.: A series of normal stages in the development of the chick embryo. J. Morph. 88, 44–92 (1951)
Hendrickson, A.E., Cowan, W.M.: Changes in the rate of axoplasmic transport during post-natal development of the rabbit's optic nerve and tract. Exp. Neurol. 30, 403–422 (1971)
James, D.W., Tresman, R.L.: The surface coats of chick dorsal root ganglion cells in vitro. J. Neurocytol. 1, 383–395 (1972)
Karlsson, J.-O., Sjöstrand, J.: Rapid intracellular transport of fucose-containing glycoproteins in retinal ganglion cells. J. Neurochem. 18, 2209–2216 (1971)
Kopriwa, B.M., Leblond, C.P.: Improvements in the coating technique of radioautography. J. Histochem. Cytochem. 10, 269–284 (1962)
Marchisio, P. C., Sjöstrand, J.: Radioautographic evidence for protein transport along the optic pathway of early chick embryos. J. Neurocytol. 1, 101–108 (1972)
Marchisio, P.C., Sjöstrand, J., Aglietta, M., Karlsson, J.-O.: The development of axonal transport of proteins and glycoproteins in the optic pathway of chick embryos. Brain Res. 63, 273–284 (1973)
Margolis, R.K., Margolis, R.U.: Disposition of fucose in brain. J. Neurochem. 19, 1023–1030 (1972)
Pysh, J. J., Wiley, R.G.: Synaptic vesicle depletion and recovery in cat sympathetic ganglia electrically stimulated in vivo. Evidence for transmitter secretion by exocytosis. J. Cell Biol. 60, 365–374 (1974)
Quarles, R.H., Brady, R.O.: Synthesis of glycoproteins and gangliosides in developing rat brain. J. Neurochem. 18, 1806–1820 (1971)
Rambourg, A., Leblond, C.P.: Electron microscope observations on the carbohydrate-rich cell coat present at the surface of cells in the rat. J. Cell Biol. 32, 27–53 (1967)
Sedlacek, J.: Development of optic evoked potentials in chick embryos. Physiol. bohemoslov. 16, 531–537 (1967)
Singer, S. J., Nicolson, G.L.: The fluid mosaic model of the structure of cell membranes. Science 175, 720–731 (1972)
Zatz, M., Barondes, S.H.: Fucose incorporation into glycoproteins of mouse brain. J. Neurochem. 17, 157–163 (1970)
Zatz, M., Barondes, S. H.: Rapid transport of fucosyl glycoproteins to nerve endings in mouse brain. J. Neurochem. 18, 1125–1133 (1971)
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This investigation was sponsored by the Swedish-Italian Research Group of Neurobiology. P.C.M. received financial support from Consiglio Nazionale delie Ricerche (C.N.R., Rome); J.S. was supported by grants from the Swedish Medical Research (no. B74-13X-2226-08C). We are indebted to Mrs. Marie-Louise Eskilson for her careful technical assistance and to Mr. Baldassarre Russo for his skilful help in photography.
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Gremo, F., Sjöstrand, J. & Marchisio, P.C. Radioautographic analysis of 3H-fucose labelled glycoproteins transported along the optic pathway of chick embryos. Cell Tissue Res. 153, 465–476 (1974). https://doi.org/10.1007/BF00231541
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DOI: https://doi.org/10.1007/BF00231541