Axon-regenerating retinal ganglion cells in adult rats synthesize the cell adhesion molecule L1 but not TAG-1 or SC-1

Molecular and Cellular Neurosciences

Volumn 9, Issue 2, 1997, Pages 116-131

  Jung, Marion ^a   Petrausch, Barbara ^a   Stuermer, Claudia A O ^a  

^a UNIVERSITY OF KONSTANZ   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CELL ADHESION MOLECULE; NEUROMODULIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ARTICLE; CELL ADHESION; CONTROLLED STUDY; FEMALE; NERVE FIBER REGENERATION; NERVE GRAFT; NONHUMAN; OPTIC NERVE LESION; PRIORITY JOURNAL; PROTEIN INDUCTION; RAT; RETINA GANGLION CELL;

ANIMALIA;

EID: 0030859064     PISSN: 10447431     EISSN: None     Source Type: Journal    
DOI: 10.1006/mcne.1997.0611     Document Type: Article

References (76)

1. Aguayo A. J., Rasminsky M., Bray G. M., Carbonetto S., McKerracher L., Villegas-Pérez M. P., Vidal-Sanz M., Carter D. A. Degenerative and regenerative responses of injured neurons in the central nervous system of adult mammals. Philos. Trans. R. Soc. London (Biol.). 331:1991;337-343.
2. Bähr M., Vanselow J., Thanos S. In vitro. Exp. Brain Res. 73:1988;393-401.
3. Bähr M., Eschweiler G. E., Wolburg H. Precrushed sciatic nerve grafts enhance survival and axonal regrowth of retinal ganglion cells in adult rats. Exp. Neurol. 116:1992;13-22.
4. Bartsch U., Kirchhoff F., Schachner M. Immunohistochemical localization of the adhesion molecules L1, N-CAM, and MAG in the developing and adult optic nerve of mice. J. Comp. Neurol. 284:1989;451-462.
5. Bastmeyer M., Schlosshauer B., Stuermer C. A. O. The spatiotemporal distribution of N-CAM in the retinotectal pathway of adult goldfish detected by the monoclonal antibody D3. Development. 108:1990;299-311.
6. Bastmeyer M., Bähr M., Stuermer C. A. O. Fish optic nerve oligodendrocytes support axonal regeneration of fish and mammalian retinal ganglion cells. Glia. 8:1993;1-12.
7. Bastmeyer M., Ott H., Leppert C. A., Stuermer C. A. O. Fish E587 glycoprotein, a member of the L1 family of cell adhesion molecules, participates in axonal fasciculation and the age-related order of ganglion cell axons in the goldfish retina. J. Cell Biol. 130:1995;969-976.
8. Bastmeyer M., Ott H., Laessing U., Stuermer C. A. O. Functional characterization of two cell adhesion molecules - the E587 antigen and neurolin - during zebrafish CNS development. Soc. Neurosci. Abstr. 22:1996;1714.
9. Bates C. A., Meyer R. L. The neurite-promoting effect of laminin is mediated by different mechanisms in embryonic and adult regenerating mouse optic axons in vitro. Dev. Biol. 181:1997;91-101.
10. Benowitz L. I., Lewis E. R. Increased transport of 44,000 to 49,000-dalton acidic proteins during regeneration of the goldfish optic nerve: A two-dimensional gel analysis. J. Neurosci. 3:1983;2153-2163.
11. Bernhardt R. R., Tongiorgi E., Anzini P., Schachner M. Increased expression of specific recognition molecules by retinal ganglion cells and by optic nerve glia accompanies the successful regeneration of retinal axons in adult zebrafish. J. Comp. Neurol. 376:1996;253-264.
12. Bock E., Richter-Landsberg C., Faissner A., Schachner M. Demonstration of immunocytochemical identity between the nerve growth factor-inducible large external (NILE) glycoprotein and the cell adhesion molecule L1. EMBO J. 4:1985;2765-2768.
13. Breitschopf H., Suchanek G., Gould R. M., Colman D. R., Lassmann H. In situ. Acta Neuropathol. 84:1992;581-587.
14. Brümmendorf T., Rathjen F. G. Cell Adhesion Molecules. 1. Immunoglobulin Superfamily. 1994;Academic Press, London.
15. Brümmendorf T., Rathjen F. G. Structure/function relationships of axon-associated adhesion receptors of the immunoglobulin superfamily. Curr. Opin. Neurobiol. 6:1996;584-593.
16. Bunge R. P., Hopkins J. M. The role of peripheral and central neuroglia in neural regeneration in vertebrates. Semin. Neurosci. 2:1990;509-518.
17. Burns F. R., von Kannen S., Guy L., Raper J. A., Kamholz J., Chang S. DM-GRASP, a novel immunoglobulin superfamily axonal surface protein that supports neurite extension. Neuron. 7:1991;209-220.
18. Chang S., Rathjen F. G., Raper J. A. Extension of neurites on axons is impaired by antibodies against specific neural cell surface glycoproteins. J. Cell Biol. 104:1987;355-362.
19. Clarke P. G. H. Neuronal death in the development of the vertebrate nervous system. Trends Neurosci. 8:1985;345-349.
20. Curtis R., Stewart H. J. S., Wilkin G. P., Mirsky R., Jessen K. R. GAP-43 is expressed by nonmyelin-forming Schwann cells of the PNS. J. Cell Biol. 116:1992;1455-1464.
21. David S., Aguayo A. J. Axonal regeneration after crush injury of rat central nervous system fibres innervating peripheral nerve grafts. J. Neurocytol. 14:1985;1-12.
22. DeBernardo A. P., Chang S. Heterophilic interactions of DM-GRASP: GRASP-NgCAM interactions involved in neurite extension. J. Cell Biol. 133:1996;657-666.
23. Dezawa M., Nagano T. Immunohistochemical localization of cell adhesion molecules and cell-cell contact proteins during regeneration of the rat optic nerve induced by sciatic nerve autotransplantation. Anat. Rec. 246:1996;114-126.
24. Dodd J., Morton S., Karagogeos D., Yamamoto M., Jessell T. M. Spatial regulation of axonal glycoprotein expression on subsets of embryonic spinal neurons. Neuron. 1:1988;105-116.
25. Doherty P., Walsh F. S. Signal transduction events underlying neurite outgrowth stimulated by cell adhesion molecules. Curr. Opin. Neurobiol. 4:1994;49-55.
26. Doster S. K., Lozano A. M., Aguayo A. J., Willard M. B. Expression of the growth-associated protein GAP-43 in adult rat retinal ganglion cells following axon injury. Neuron. 6:1991;635-647.
27. Fawcett J. W., Keynes R. J. Peripheral nerve regeneration. Annu. Rev. Neurosci. 13:1992;43-60.
28. 1. Neuron. 12:1994;675-690.
29. Furley A. J., Manalo D., Karagogeos D., Dodd J., Jessell T. M. The axonal glycoprotein is an immunoglobulin superfamily member with neurite outgrowth-promoting activity. Cell. 61:1990;157-170.
30. Gaze R. M. The Formation of Nerve Connections. 1970;Academic Press, London.
31. Giordano S., Laessing U., Ankerhold R., Lottspeich F., Stuermer C. A. O. Molecular characterization of E587 antigen: An axonal recognition molecule expressed in the goldfish central nervous system. J. Comp. Neurol. 377:1997;286-297.
32. Grafstein B. The retina as a regenerating organ. The Retina: A Model for Cell Biology Studies. 1986;Academic Press, New York. p. 275-335.
33. Grafstein B., McQuarrie I. G. Role of the nerve cell body in axonal regeneration. Cotman C. W. Neuronal Plasticity. 1978;155-195 Raven Press, New York.
34. Halfter W., Reckhaus W., Kröger S. Nondirected axonal growth on basal lamina from avian embryonic neural retina. J. Neurosci. 8:1987;3712-3722.
35. Kapfhammer J., Christ F., Schwab M. E. The expression of GAP-43 and synaptophysin in the developing rat retina. Dev. Brain Res. 80:1994;251-260.
36. Karagogeos D., Morton S. B., Casano F., Dodd J., Jessell T. M. Developmental expression of the axonal glycoprotein TAG-1: Differential regulation by central and peripheral neurons in vitro. Development. 112:1991;51-67.
37. Kuhn T. B., Stoeckli E. T., Condrau F. G., Rathjen F. G., Sonderegger P. Neurite outgrowth on immobilized axonin-1 is mediated by heterophilic interaction with L1 (G4). J. Cell Biol. 115:1991;1113-1126.
38. Kunz S., Ziegler U., Kunz B., Sonderegger P. A switch in intracellular signalling after clustering of the neural cell adhesion molecules axonin-1 and NgCAM during neurite fasciculation. J. Cell Biol. 1996.
39. Laessing U., Giordano S., Stecher B., Lottspeich F., Stuermer C. A. O. Molecular characterization of fish neurolin: A growth-associated cell surface protein and member of the immunoglobulin superfamily in the fish retinotectal system with similarities to chick protein DM-GRASP/SC-1/BEN. Differentiation. 56:1994;21-29.
40. Laessing U., Stuermer C. A. O. Spatiotemporal pattern of retinal ganglion cell differentiation revealed by the expression of neurolin in embryonic zebrafish. J. Neurobiol. 29:1996;65-74.
41. Lemansky P., Fatemi S. H., Gorican B., Meyale S., Rossero R., Tartakoff A. M. Dynamics and longevity of the glycolipid-anchored membrane protein Thy-1. J. Cell Biol. 110:1990;1525-1531.
42. Lemmon V., Farr K. L., Lagenaur C. L1-mediated axon outgrowth occurs via a homophilic binding mechanism. Neuron. 2:1989;1597-1603.
43. McKerracher L., Vidal-Sanz M., Aguayo A. J. Slow transport rates of cytoskeletal proteins change during regeneration of axotomized retinal neurons in adult rats. J. Neurosci. 10:1990;641-648.
44. Mohajeri M. H., Bartsch U., Van der Putten H., Sansig G., Mucke L., Schachner M. Neurite outgrowth on non-permissive substrates in vitro is enhanced by ectopic expression of the neural adhesion molecule L1 by mouse astrocytes. Eur. J. Neurosci. 8:1996;1085-1097.
45. Needham L. K., Tennekoon G. I., McKhann G. M. Selective growth of rat Schwann cells in neuron- and serum-free primary cultures. J. Neurosci. 7:1987;1-9.
46. Paschke K. A., Lottspeich F., Stuermer C. A. O. Neurolin, a cell surface glycoprotein on growing retinal axons in the goldfish visual system, is reexpressed during retinal axonal regeneration. J. Cell Biol. 117:1992;864-875.
47. Pennypacker K., Fischer J., Levitt P. Early in vitro genesis and differentiation of axons and dendrites by hippocampal neurons analyzed quantitatively with neurofilament-H and microtubule-associated protein-2 antibodies. Exp. Neurol. 111:1991;25-34.
48. Pollerberg E., Sadoul R., Goridis C., Schachner M. Selective expression of the 180 kD component of the neural cell adhesion molecule NCAM during development. J. Cell Biol. 101:1985;1921-1929.
49. Pollerberg G. E., Mack T. G. A. Cell adhesion molecule SC1/DMGRASP is expressed on growing axons of retina ganglion cells and is involved in mediating their extension on axons. Dev. Biol. 165:1994;670-687.
50. Prince J. T., Alberti L., Healy P. A., Nauman S. J., Stallcup W. B. Molecular cloning of NILE glycoprotein and evidence for its continued expression in mature rat CNS. J. Neurosci. Res. 30:1991;567-581.
51. Prince J. T., Nishiyama A., Healy P. A., Beasley L., Stallcup W. B. Expression of the F84.1 glycoprotein in the spinal cord and cranial nerves of the developing rat. Dev. Brain Res. 68:1992;193-201.
52. Rader C., Stoeckli E. T. U., Ziegler U., Osterwalder T., Kunz B., Sonderegger P. Cell-cell adhesion by homophilic interaction of the neuronal recognition molecules axonin-1. Eur. J. Biochem. 215:1993;133-141.
53. Rathjen F. G., Schachner M. Immunocytological and biochemical characterization of a new neuronal cell surface component (L1 antigen) which is involved in cell adhesion. EMBO J. 3:1984;1-10.
54. Rathjen F. G., Wolff J. M., Frank R., Bonhoeffer F., Rutishauser U. Membrane glycoproteins involved in neurite fasciculation. J. Cell Biol. 104:1987;343-353.
55. Reh T. A., Tetzlaff W., Ertmaier A., Zwiers H. Developmental study of the expression of B50/GAP-43 in rat retina. J. Neurobiol. 24:1993;949-958.
56. Ruegg M. A., Stoeckli E. T., Lanz R. B., Streit P., Sonderegger P. A homologue of the axonally secreted protein axonin-1 is an integral memberane protein of nerve fiber tracts involved in neurite fasciculation. J. Cell Biol. 109:1989;2363-2378.
57. Schaden H., Stuermer C. A. O., Bähr M. GAP-43 immunoreactivity and axon regeneration in retinal ganglion cells of the rat. J. Neurobiol. 25:1994;1570-1578.
58. Schwab M. E., Kapfhammer J., Bandtlow C. E. Inhibitors of neurite growth. Annu. Rev. Neurosci. 16:1993;565-595.
59. Schwalb J. M., Gu M.-f., Stuermer C. A. O., Bastmeyer M., Hu G.-f., Boulis N., Irwin N., Benowitz L. J. Optic nerve glia secrete a low-molecular-weight factor that stimulates retinal ganglion cells to regenerate axons in goldfish. Neuroscience. 72:1996;901-910.
60. Shreyer D., Skene J. H. P. Fate of GAP-43 in ascending spinal axons of DRG neurons after peripheral nerve injury: Delayed accumulation and correlation with regenerative potential. J. Neurosci. 12:1991;3738-3751.
61. Seilheimer B., Schachner M. Studies of adhesion molecules mediating interactions between cells of peripheral nervous system indicate a major role for L1 in mediating sensory neuron growth on Schwann cells in culture. J. Cell Biol. 107:1988;341-351.
62. Skene J. H. P. Axonal growth-associated proteins. Annu. Rev. Neurosci. 12:1989;127-156.
63. Skene J. H. P. Retrograde pathways controlling expression of a major growth cone component in the adult CNS. Letourneau P. C., Kater S. B., Macagno E. R. The Nerve Growth Cone. 1991;463-475 Raven Press, New York.
64. Stallcup W. B., Beasley L. L. Involvement of the nerve growth factor-inducible large external glycoprotein (NILE) in neurite fasciculation in primary cultures of rat brain. Proc. Natl. Acad. Sci. USA. 82:1985;1276-1280.
65. Stallcup W. B., Beasley L. L., Levine J. M. Antibody against nerve growth factor-inducible large external (NILE) glycoprotein labels nerve fiber tracts in the developing rat nervous system. J. Neurosci. 5:1985;1090-1101.
66. Stoeckli E. T., Kuhn T. B., Duc C. O., Ruegg M. A., Sonderegger P. The axonally secreted protein axonin-1 is a potent substratum for neurite growth. J. Cell Biol. 112:1991;449-455.
67. Stuermer C. A. O., Bastmeyer M., Bähr M., Strobel G., Paschke K. Trying to understand axonal regeneration in the CNS of fish. J. Neurobiol. 23:1992;537-550.
68. Tanaka H., Matsui T., Agata A., Tomura M., Kubota I., McFarland K. C., Kohr B., Lee A., Phillips H. S., Shelton D. L. Molecular cloning and expression of a novel adhesion molecule, SC1. Neuron. 7:1991;535-545.
69. Vidal-Sanz M., Bray G. M., Villégas-Perez M. P., Thanos S., Aguayo A. J. Axonal regeneration and synapse formation in thesuperior colliculus. J. Neurosci. 7:1987;2894-2909.
70. Vielmetter J., Lottspeich F., Stuermer C. A. O. The monoclonal antibody E587 recognizes growing (new and regenerating) retinal axons in the goldfish retinotectal pathway. J. Neurosci. 11:1991;3581-3593.
71. Villegas-Pérez M. P., Vidal-Sanz M., Bray G. M., Aguayo A. J. Influences of peripheral nerve grafts on the survival and regrowth of axotomized retinal ganglion cells in adult rats. J. Neurosci. 8:1988;265-280.
72. Villegas-Pérez M. P., Vidal-Sanz M., Rasminsky M., Bray G. M., Aguayo A. J. Rapid and protracted phases of retinal ganglion cell loss follow axotomy in the optic nerve of adult rats. J. Neurobiol. 24:1992;23-36.
73. Wanner M., Lang D. M., Bandtlow C. E., Schwab M. E., Bastmeyer M., Stuermer C. A. O. Reevaluation of the growth-permissive substrate properties of goldfish optic nerve myelin and myelin proteins. J. Neurosci. 15:1995;7500-7508.
74. Westerfield M. The Zebrafish Book: A Guide for the Laboratory Use of Zebrafish (Brachydanio rerio). 1994;Univ. of Oregon Press, Eugene.
75. Wilkinson D. G. In Situ Hybridization: A Practical Approach. 1992;IRL Press at Oxford Univ. Press, Oxford.
76. Yamagata M., Herman J.-P., Sanes J. R. Lamina-specific expression of adhesion molecules in developing chick optic tectum. J. Neurosci. 15:1995;4556-4571.