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A breakdown of the blood-brain barrier is associated with optic nerve regeneration in the frog

Published online by Cambridge University Press:  02 June 2009

M. Tennant
Affiliation:
Department of Anatomy and Human Biology, The University of Western Australia, Nedlands, Australia
L. D. Beazley
Affiliation:
Neurobiology Laboratory, Department of Psychology, The University of Western Australia, Nedlands, Australia

Abstract

We have examined the integrity of the blood-brain barrier during optic nerve regeneration in the frog Liloria (Hyla) moorei using rhodamine B-labeled bovine serum albumin (RBA). A transient localized breakdown of the blood-brain barrier was observed between 1 and 5 weeks after extracranial optic nerve crush. The zone of breakdown progressed along the experimental optic nerve, ascended the opposite optic tract, and swept rostro-caudally across the tectum contralateral to the crushed nerve. By 7 weeks, the blood-brain barrier was once again intact along the length of the optic pathway. In a concurrent series of frogs, regenerating optic axons were visualized by anterograde transport of horseradish peroxidase (HRP). At each stage examined, the region reached by the front of regenerating axons corresponded to that in which the blood-brain barrier had been shown to break down.

In contrast to the results after nerve crush, the blood-brain barrier remained intact along the length of the optic pathway following optic nerve ligation to prevent regeneration. We conclude that the breakdown of the blood-brain barrier which occurs during optic nerve regeneration in the frog is triggered by the regenerating axons.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1992

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References

Beazley, L.D. (1984). Formation of specific neuronal connections in the visual system of lower vertebrates. In Current Topics in Research on Synapses. Vol. 1, ed. Jones, D.G., pp. 55117. New York: Liss.Google Scholar
Carlstedt, T., Dalsgaard, C.J. & Molander, C. (1987). Regrowth Of Lesioned Dorsal Root Nerve Fibers Into The Spinal Cord Of Neonatal Rats. Neuroscience Letters 74, 1418.CrossRefGoogle ScholarPubMed
Darby, J.E., Carr, R.A. & Beazley, L.D. (1990). Retinal ganglion cell death during regeneration of the frog optic nerve is not accompanied by appreciable cell loss from the inner nuclear layer. Anatomy and Embryology 182, 487492.CrossRefGoogle Scholar
Gaze, R.M. (1970). The Formation of Nerve Connections. London, UK: Academic Press.Google Scholar
Harvey, A.R., Rush, R.A. & Keating, P.J. (1988). Cultured fetal tectal tissue grafted to the midbrain of newborn rats: Morphology of grafts and innervation by host retinal and cortical axons. Brain Research 462, 8998.CrossRefGoogle Scholar
Humphrey, M.F. & Beazley, L.D. (1982). An electrophysiological study of early retinotectal projection patterns during optic nerve regeneration in Hyla moorei. Brain Research 239, 595602.CrossRefGoogle ScholarPubMed
Humphrey, M.F. & Beazley, L.D. (1985). Retinal gangtion cell death during optic nerve regeneration in the frog Hyla moorei. Journal of Comparative Neurology 236, 382402.CrossRefGoogle ScholarPubMed
Humphrey, M.F., Darby, J.E. & Beazley, L.D. (1989). Prevention of optic nerve regeneration in the frog Hyla moorei transiently delays the death of some ganglion cells. Journal of Comparative Neurology 279, 187198.CrossRefGoogle ScholarPubMed
Jacobson, M. (1978). DevelopmentalNeurobiology. New York: Plenum Press.Google Scholar
Kiernan, J.A. & Contestabile, A. (1980). Vascular permeability associated with axonal regeneration in the optic system of the goldfish. Acta Neuropathologica (Berlin) 51, 3945.CrossRefGoogle ScholarPubMed
Kiernan, J.A. (1979). Hypothesis concerned with axonal regeneration in the mammalian nervous system. Biological Review 54, 155197.CrossRefGoogle Scholar
Kiernan, J.A. (1985). Axonal and vascular changes following injury to the rat's optic nerve. Journal of Anatomy 141, 139154.Google Scholar
Kuljis, R.O. & Karten, H.J. (1983). Modifications on the laminar of peptide-like immunoreactivity in the Anuran optic tectum following retinal deafferentation. Journal of Comparative Neurology 217, 239251.CrossRefGoogle ScholarPubMed
Lossinsky, A.S., Vorbrodt, A.W. & Wisniewski, H.M. (1986). Characterization of endothelial cell transport in the developing mouse blood-brain barrier. Developmental Neuroscience 8, 6175.CrossRefGoogle ScholarPubMed
Lyon, M.J. & Stelzner, D.J. (1987). Tests of the regenerative capacity of tectal efferent axons in the frog, Rana pipiens. Journal of Comparative Neurology 255, 511525.CrossRefGoogle ScholarPubMed
Malmgren, L.T. & Olsson, Y. (1977). A sensitive histochemical method for light- and electron-microscopic demonstration of horseradish peroxidase. Journal of Histochemistry and Cytochemistry 25, 12801283.CrossRefGoogle ScholarPubMed
Mellick, R.S. & Cavanagh, J.B. (1968). Changes in blood vessel permeability during degeneration and regeneration in peripheral nerves. Brain 91, 141160.CrossRefGoogle ScholarPubMed
Murray, M. (1977). Delayed regeneration of the retino-diencephalic projections in the goldfish, Carassius auratus. Brain Research 125, 149153.CrossRefGoogle ScholarPubMed
Murray, M. (1982). A quantitative study of regenerative sprouting by optic axons in goldfish. Journal of Comparative Neurology 209, 352362.CrossRefGoogle ScholarPubMed
Olsson, Y. (1966). Studies on vascular permeability in peripheral nerves. I. Distribution of circulating fluoresent serum albumin in normal, crushed, and sectioned rat sciatic nerve. Ada Neuropathologica 7, 115.CrossRefGoogle Scholar
Peters, A., Palay, S.L. & Webster, H.F. (1976). The Fine Structure of the Nervous System. Philadelphia, Pennsylvania: Saunders.Google Scholar
Ramon-Y-Cajal, S. (1928). Degeneration and Regeneration of the Nervous System, (edited and translated by May, R.M.). New York: Hafner.Google Scholar
Rapoport, S.I. (1976). Blood-Brain Barrier in Physiology and Medicine. New York: Raven Press.Google Scholar
Risling, M., Cullheim, S. & Hildebrand, C. (1983). Reinnervation of the ventral root L7 from ventral horn neurons following intramedullary axotomy in adult cats. Brain Research 280, 1523.CrossRefGoogle ScholarPubMed
Risling, M., Linda, H., Cullheim, S. & Franson, P. (1989). A persistent defect in the blood-brain barrier after ventral funiculus lesion in adult cats: Implications for CNS regeneration? Brain Research 494, 1321.CrossRefGoogle ScholarPubMed
Sheard, P.W. & Beazley, L.D. (1988). Retinal ganglion cell death is not prevented by application of tetrodotoxin during optic nerve regeneration in the frog Hyla moorei. Vision Research 28, 461470.CrossRefGoogle Scholar
Sievers, J., Hausmann, B. & Berry, M. (1989). Fetal brain grafts rescue adult retinal ganglion cells from axotomy-induced cell death. Journal of Comparative Neurology 281, 467478.CrossRefGoogle ScholarPubMed
Sparrow, J.R. & Kiernan, J.A. (1981). Endoneurial Vascular Permeability In Degenerating And Regenerating Peripheral Nerves. Ada Neuropathologica (Berlin) 53, 181188.CrossRefGoogle Scholar
Sperry, R.W. (1963). Chemoaffinity in the orderly growth of nerve fiber patterns and connections. Proceedings of the National Academy of Sciences of the U.S.A. 50, 703709.CrossRefGoogle ScholarPubMed
Stelzner, D.J. & Strauss, J.A. (1986). A quantitative analysis of frog optic nerve regeneration: Is retrograde ganglion cell death or collateral axonal loss related to selective reinnervation? Journal of Comparative Neurology 245, 83106.CrossRefGoogle ScholarPubMed
Tennant, M. & Beazley, L.D. (1991). Regenerating optic axons stimulate a breakdown of the blood-brain barrier in the frog. Proceedings of the Australian Neuroscience Society 2, 48.Google Scholar
Vidal-Sanz, M., Bray, G.M., Villegas-Perez, M.P., Thanos, S. & Aguayo, A.J. (1987). Axonal regeneration and synapse formation in the superior colliculus by retinal ganglion cells in the adult rat. Journal of Neuroscience 7, 28942909.CrossRefGoogle ScholarPubMed
Villegas-Perez, M.P., Vidal-Sanz, M., Bray, G.M. & Aguayo, A.J. (1988). Influences of peripheral nerve grafts on the survival and regrowth of axotomized retinal ganglion cells in adult rats. Journal of Neuroscience 8, 265280.CrossRefGoogle ScholarPubMed