Hostname: page-component-848d4c4894-tn8tq Total loading time: 0 Render date: 2024-07-04T21:49:04.208Z Has data issue: false hasContentIssue false
  • English
  • Français

Regenerating axons from adult chick retinal ganglion cells recognize topographic cues from embryonic central targets

Published online by Cambridge University Press:  02 June 2009

Jens Vanselow ,
Bernhard Müller  and
Solon Thanos
Jens Vanselow
Affiliation:
Max-Planck-Institute for Developmental Biology, Tübingen, Germany
Bernhard Müller
Affiliation:
Max-Planck-Institute for Developmental Biology, Tübingen, Germany
Solon Thanos
Affiliation:
Department of Ophthalmology, University of Tübingen, School of Medicine, Tübingen, Germany
Get access Rights & Permissions [Opens in a new window]

Abstract

We investigated whether regenerating mature axons recapitulate embryonic features essential to successful reconnectivity within the injured nervous system. Strips from embryonic and adult chick retinae were cultured, and outgrowing axons were examined morphometrically and immunohistochemically. In addition, the target-recognition properties of adult neurites were analyzed. Regenerating adult axons elongate on a poly-L-lysine/laminin substratum with a speed about one order of magnitude slower than that of embryonic axons. Morphologically, adult axonal tips differ dramatically from embryonic growth cones in that they possess only filopodial extensions whereas embryonic growth cones possess both lamellipodial and filopodial processes. Both embryonic and adult neurites express the growth-associated protein GAP-43. When cultured on alternating stripes of anterior and posterior embryonic tectal membranes, both adult and embryonic retinal axons distinguish between the two membrane preparations. Our results demonstrate that during axonal regeneration the mature neurons express embryonic properties that are involved in the recognition of tectal positional cues.

Keywords

RetinaRegenerationGanglion cellsPositional markersExplants
Type
Research Articles
Information
Visual Neuroscience , Volume 6 , Issue 6 , June 1991 , pp. 569 - 576
Copyright
Copyright © Cambridge University Press 1991

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Agranoff, B.W., Field, P. & Gaze, R.M. (1976). Neurite outgrowth from explanted Xenopus retina: an effect of prior optic nerve section. Brain Research 113, 225–234.CrossRefGoogle ScholarPubMed
Aguayo, A.J. (1985). Axonal regeneration from injured neurons in the adult mammalian central nervous system. In Synaptic Plasticity, ed. Cotman, C.W., pp. 457–484. New York: Guilford Press.Google Scholar
Allsopp, T.E. & Moss, D.J. (1989). A developmentally regulated chicken neuronal protein associated with the cortical cytoskeleton. Journal of Neuroscience 9, 13–24.CrossRefGoogle ScholarPubMed
Argiro, V., Bunge, M.B. & Johnson, M.I. (1984). Correlation between growth-cone form and movement and their dependence on neuronal age. Journal of Neuroscience 4, 3051–3062.CrossRefGoogle ScholarPubMed
Argiro, V, Bunge, M.B. & Johnson, M.I. (1985). A quantitative study of growth-cone filopodial extension. Journal of Neuroscience Research 13, 149–162.CrossRefGoogle ScholarPubMed
Bähr, M., Vanselow, J. & Thanos, S. (1988). In vitro regeneration of adult rat ganglion cell axons from retinal explants. Experimental Brain Research 73, 393–401.CrossRefGoogle ScholarPubMed
Benowitz, L.I. & Schmidt, J.T. (1987). Activity-dependent sharpening of the regenerating retinotectal projection in goldfish: relationship to the expression of growth-associated proteins. Brain Research 417, 118–126.CrossRefGoogle Scholar
Benowitz, L. I., Apostolides, P. J., Perrone-Bizzozero, N.J., Fincklestein, S.P. & Zwiers, H. (1988). Anatomical distribution of the growth-associated proteins GAP-43/B-50 in the adult rat brain. Journal of Neuroscience 8, 339–352.CrossRefGoogle ScholarPubMed
Berry, M., Rees, L. & Sievers, J. (1986). Regeneration of axons in the mammalian visual system. Experimental Brain Research (Supp.) 13, 18–33.Google Scholar
Bonhoeffer, F. & Gierer, A. (1984). How do retinal axons find their targets on the tectum? TINS 7, 378–381.Google Scholar
Bonhoeffer, F. & Huf, J. (1982). In vitro experiments on axon guidance demonstrating an anterior-posterior gradient on the tectum. EMBO Journal 4, 427–431.CrossRefGoogle Scholar
Bonhoeffer, F. & Huf, J. (1985). Position-dependent properties of retinal axons and their growth cones. Nature 315, 409–410.CrossRefGoogle ScholarPubMed
Cohen, J., Burne, J.F., Winter, J. & Bartlett, P. (1986), Retinal ganglion cells lose response to laminin with maturation. Nature 322, 465–467.CrossRefGoogle ScholarPubMed
Cox, E.C., Müller, B. & Bonhoeffer, F. (1990). Axonal guidance in the chick visual system: posterior tectal membranes induce collapse of growth cones from the temporal retina. Neuron 2, 31–37.CrossRefGoogle Scholar
Godement, P. & Bonhoeffer, F. (1989). Cross-species recognition of tectal cues by retinal fibers in vitro. Development 106, 313–320.CrossRefGoogle ScholarPubMed
Godement, P., Vanselow, J., Thanos, S. & Bonhoeffer, F. (1987). A study of developing visual systems with a new method for staining neurones and their processes in fixed tissue. Development 101, 697–713.CrossRefGoogle ScholarPubMed
Goverdhan-Löbbert, A. (1989). Einfluss der plamamembranen und membrankomponenten auf das axonale wachstum. Dissertation, Eberhard-Karls Universität, Tübingen.Google Scholar
Johnson, A.R., Wigley, C.B., Gregson, N.A., Cohen, J. & Berry, M. (1988). Neither laminin nor prior optic nerve section are essential for the regeneration of adult mammalian retinal ganglion cell axons in vitro. Journal of Neurocytology 17, 95–104.CrossRefGoogle ScholarPubMed
Kapfhammer, J.P., Grunewald, B.E. & Raper, J.A. (1986). The selective inhibition of growth-cone extension by specific neurites in culture. Journal of Neuroscience 6(9), 2527–2534.CrossRefGoogle ScholarPubMed
Kapfhammer, J.K.P. (1988). Zeitraffer-video-untersuchungen zum verhalten einzelner wachstumskegel aus nervengewebs-explantaten des embryonalen huehnchens bei kontakt mit neuronalen oberflächen in vitro. Dissertation, Eberhard-Karls Universität, Tübingen.Google Scholar
Keirstead, S.A., Rasminsky, M., Fukuda, Y., Carter, D.A., Aguayo, A.J. & Vidal-Sanz, M. (1989). Electrophysiologic responses in hamster superior colliculus evoked by regenerating retinal axons. Science 246, 255–257.CrossRefGoogle ScholarPubMed
Mason, C.A. (1985). Growing tips of embryonic cerebellar axons in vivo. Journal of Neuroscience Research 13, 55–73.CrossRefGoogle ScholarPubMed
Meiri, K.F., Pfenninger, K.H. & Willard, M.B. (1988). Growth-ssociated protein, GAP-43, a polypeptide that is induced when neurons extend axons, is a component of growth cones and corresponds to pp46, a major polypeptide of a subcellular fraction enriched in growth cones. Proceedings of the National Academy of Science of the U.S.A. 83, 3537–3541.CrossRefGoogle Scholar
Miotke, J., Meyer, R.L. & Benowitz, L.I. (1989). GAP-43 expression in regenerating adult optic fibers in vitro. Society for Neuroscience Abstracts 15, 1224.Google Scholar
Moss, D.J., Fernyhough, K., Chapman, K., Baizer, L., Bray, D. & Allsopp, T. (1990). Chicken growth-associated protein GAP-43 is tightly bound to the actin-rich neuronal membrane skeleton. Journal of Neurochemistry 54, 729–736.CrossRefGoogle Scholar
Muchnick, N. & Hibbard, E. (1980). Avian retinal ganglion cells resistant to degeneration after optic nerve lesion. Experimental Neurology 68, 205–216.CrossRefGoogle ScholarPubMed
Needham, L.K., Tennekoon, G.I. & McKhann, G.M. (1987). Selective growth of rat Schwann cells in neuron- and serum-free primary culture. Journal of Neuroscience 7, 1–9.CrossRefGoogle ScholarPubMed
Ng, S.C., De, La Monte S.M., Conboy, G.L., Karns, L.R. & Fishman, M.C. (1988). Cloning of human GAP-43: growth association and ischemic resurgence. Neuron, 1, 133–139.CrossRefGoogle ScholarPubMed
Nordlander, R.H. (1987). Axonal growth cones in the developing &hibian spinal cord. Journal of Comparative Neurology 263, 485–496.CrossRefGoogle ScholarPubMed
Rathjen, F.G., Wolff, J.M., Frank, R., Bonhoeffer, F. & Rutishauser, U. (1987). Membrane glycoproteins involved in neurite fasciculation. Journal of Cell Biology 104, 343–353.CrossRefGoogle ScholarPubMed
Schnell, L. & Schwab, M.E. (1990) Axonal regeneration in the rat spinal cord produced by an antibody against myelin-associated neurite growth inhibitors. Nature 343, 269–270.CrossRefGoogle ScholarPubMed
Schwab, M.E. & Caroni, P. (1988). Oligodendrocytes and CNS myelin are non-permissive substrates for neurite growth and fibroblast spreading in vitro. Journal of Neuroscience 8, 2381–2393.CrossRefGoogle Scholar
Skene, J.H.P. & Willard, M. (1981). Axonally transported proteins associated with axon growth in rabbit central and peripheral nervous system. Journal of Cell Biology 89, 96–103.CrossRefGoogle Scholar
Skene, J.H.P. (1989). Axonal growth-associated proteins. Annual Review of Neuroscience 12, 127–156.CrossRefGoogle ScholarPubMed
Thanos, S. (1988). Alterations in the morphology of ganglion cell dendrites in the adult rat retina after optic nerve transection and grafting of peripheral nerve segments. Cell Tissue Research 254, 599–609.CrossRefGoogle ScholarPubMed
Thanos, S., Bähr, M., Barde, Y.A. & Vanselow, J. (1989). Survival and axonal elongation of adult rat retinal ganglion cells: in vitro effects of lesioned sciatic nerve and brain-derived neurotrophic factor (BDNF). European Journal of Neuroscience 1, 19–26.CrossRefGoogle Scholar
Thanos, S. & Vanselow, J. (1990). Fetal tectal transplants in the cortex of adult rats become innervated both by retinal ganglion cell axons regenerating through peripheral nerve grafts and by cortical neurons. Rst. Neurol. Neuroscience (in press).CrossRefGoogle Scholar
Thanos, S. & Bonhoeffer, F. (1983). Investigations on development and topographic order of retinotectal axons: anterograde and retrograde staining of axons with rhodamine in vivo. Journal of Comparative Neurology 219, 420–430.CrossRefGoogle ScholarPubMed
Tosney, K.W. & Landmesser, L.T. (1985). Growth cone morphology and trajectory in the lumposacral region of the chick embryo. Journal of Neuroscience 5, 2345–2358.CrossRefGoogle ScholarPubMed
Vanselow, J., Schwab, M.E. & Thanos, S. (1990). Responses of regenerating rat retinal ganglion cell axons to contacts with central nervous myelin in vitro. European Journal of Neuroscience 2, 121–125.CrossRefGoogle ScholarPubMed
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 adult rat. Journal of Neuroscience 7, 2894–2909.CrossRefGoogle ScholarPubMed
Walter, J., Kern-Veits, B., Huf, J., Stolze, B. & Bonhoeffer, F. (1987). Recognition of position-specific properties of tectal cell membranes by retinal axons in vitro. Development 101, 685–696.CrossRefGoogle ScholarPubMed
Zuber, M.X., Goodman, D.W., Karns, L.R. & Fishman, M.C. (1989 a). The neuronal growth-associated protein GAP-43 induces filopodia in non-neuronal cells. Science 244, 1193–1195.CrossRefGoogle ScholarPubMed
Zuber, M.X., Strittmatter, S.M. & Fishman, M.C. (1989 b). A membrane-targeting signal in the amino terminus of the neuronal protein GAP-43. Nature 341, 345–348.CrossRefGoogle ScholarPubMed