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. 1995 Aug 2;130(4):969–976. doi: 10.1083/jcb.130.4.969

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

PMCID: PMC2199948  PMID: 7642712

Abstract

Axons derived from young ganglion cells in the periphery of the retinae of larval and adult goldfish are known to fasciculate with one another and their immediate forerunners, creating the typical age-related order in the retinotectal pathway. Young axons express the E587 antigen, a member of the L1 family of cell adhesion molecules. Repeated injections of Fab fragments from a polyclonal E587 antiserum (E587 Fabs) into the eye of 3.4 cm goldfish disrupted the orderly fascicle pattern of RGC axons in the retina which was preserved in controls. Instead of bundling tightly, RGC axons crossed one another, grew between fascicles and arrived at the optic disk in a broadened front. When added to RGC axons growing in vitro, E587 Fabs neutralized the preference of growth cones to elongate on lanes of E587 protein, caused defasciculation of axons which normally prefer to grow along each other when explanted on polylysine, and prevented clustering of E587 antigen at axon-axon contact sites. Monoclonal E587 antibody disturbed axonal fasciculation moderately but led to a 30% reduction in growth velocities when axons tracked other axons. Therefore we conclude that E587 antigen mediates axonal recognition, selective fasciculation and the creation of the age- related order in the fish retina.

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Selected References

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  1. Bartsch U., Kirchhoff F., Schachner M. Immunohistological localization of the adhesion molecules L1, N-CAM, and MAG in the developing and adult optic nerve of mice. J Comp Neurol. 1989 Jun 15;284(3):451–462. doi: 10.1002/cne.902840310. [DOI] [PubMed] [Google Scholar]
  2. Bastmeyer M., Schlosshauer B., Stuermer C. A. The spatiotemporal distribution of N-CAM in the retinotectal pathway of adult goldfish detected by the monoclonal antibody D3. Development. 1990 Feb;108(2):299–311. doi: 10.1242/dev.108.2.299. [DOI] [PubMed] [Google Scholar]
  3. Brümmendorf T., Rathjen F. G. Axonal glycoproteins with immunoglobulin- and fibronectin type III-related domains in vertebrates: structural features, binding activities, and signal transduction. J Neurochem. 1993 Oct;61(4):1207–1219. doi: 10.1111/j.1471-4159.1993.tb13611.x. [DOI] [PubMed] [Google Scholar]
  4. 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. 1991 Aug;7(2):209–220. doi: 10.1016/0896-6273(91)90259-3. [DOI] [PubMed] [Google Scholar]
  5. 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. 1987 Feb;104(2):355–362. doi: 10.1083/jcb.104.2.355. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Dodd J., Jessell T. M. Axon guidance and the patterning of neuronal projections in vertebrates. Science. 1988 Nov 4;242(4879):692–699. doi: 10.1126/science.3055291. [DOI] [PubMed] [Google Scholar]
  7. Doherty P., Moolenaar C. E., Ashton S. V., Michalides R. J., Walsh F. S. The VASE exon downregulates the neurite growth-promoting activity of NCAM 140. Nature. 1992 Apr 30;356(6372):791–793. doi: 10.1038/356791a0. [DOI] [PubMed] [Google Scholar]
  8. Doherty P., Williams E., Walsh F. S. A soluble chimeric form of the L1 glycoprotein stimulates neurite outgrowth. Neuron. 1995 Jan;14(1):57–66. doi: 10.1016/0896-6273(95)90240-6. [DOI] [PubMed] [Google Scholar]
  9. Easter S. S., Jr, Bratton B., Scherer S. S. Growth-related order of the retinal fiber layer in goldfish. J Neurosci. 1984 Aug;4(8):2173–2190. doi: 10.1523/JNEUROSCI.04-08-02173.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Easter S. S., Jr, Rusoff A. C., Kish P. E. The growth and organization of the optic nerve and tract in juvenile and adult goldfish. J Neurosci. 1981 Aug;1(8):793–811. doi: 10.1523/JNEUROSCI.01-08-00793.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Frei T., von Bohlen und Halbach F., Wille W., Schachner M. Different extracellular domains of the neural cell adhesion molecule (N-CAM) are involved in different functions. J Cell Biol. 1992 Jul;118(1):177–194. doi: 10.1083/jcb.118.1.177. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Furley A. J., Morton S. B., Manalo D., Karagogeos D., Dodd J., Jessell T. M. The axonal glycoprotein TAG-1 is an immunoglobulin superfamily member with neurite outgrowth-promoting activity. Cell. 1990 Apr 6;61(1):157–170. doi: 10.1016/0092-8674(90)90223-2. [DOI] [PubMed] [Google Scholar]
  13. Grenningloh G., Goodman C. S. Pathway recognition by neuronal growth cones: genetic analysis of neural cell adhesion molecules in Drosophila. Curr Opin Neurobiol. 1992 Feb;2(1):42–47. doi: 10.1016/0959-4388(92)90160-m. [DOI] [PubMed] [Google Scholar]
  14. Hortsch M., Goodman C. S. Cell and substrate adhesion molecules in Drosophila. Annu Rev Cell Biol. 1991;7:505–557. doi: 10.1146/annurev.cb.07.110191.002445. [DOI] [PubMed] [Google Scholar]
  15. Johns P. R., Easter S. S., Jr Growth of the adult goldfish eye. II. Increase in retinal cell number. J Comp Neurol. 1977 Dec 1;176(3):331–341. doi: 10.1002/cne.901760303. [DOI] [PubMed] [Google Scholar]
  16. Johns P. R. Growth of the adult goldfish eye. III. Source of the new retinal cells. J Comp Neurol. 1977 Dec 1;176(3):343–357. doi: 10.1002/cne.901760304. [DOI] [PubMed] [Google Scholar]
  17. Jouet M., Kenwrick S. Gene analysis of L1 neural cell adhesion molecule in prenatal diagnosis of hydrocephalus. Lancet. 1995 Jan 21;345(8943):161–162. doi: 10.1016/s0140-6736(95)90170-1. [DOI] [PubMed] [Google Scholar]
  18. Kaethner R. J., Stuermer C. A. Dynamics of terminal arbor formation and target approach of retinotectal axons in living zebrafish embryos: a time-lapse study of single axons. J Neurosci. 1992 Aug;12(8):3257–3271. doi: 10.1523/JNEUROSCI.12-08-03257.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Landmesser L., Dahm L., Tang J. C., Rutishauser U. Polysialic acid as a regulator of intramuscular nerve branching during embryonic development. Neuron. 1990 May;4(5):655–667. doi: 10.1016/0896-6273(90)90193-j. [DOI] [PubMed] [Google Scholar]
  20. Lemmon V., Farr K. L., Lagenaur C. L1-mediated axon outgrowth occurs via a homophilic binding mechanism. Neuron. 1989 Jun;2(6):1597–1603. doi: 10.1016/0896-6273(89)90048-2. [DOI] [PubMed] [Google Scholar]
  21. Paschke K. A., Lottspeich F., Stuermer C. A. Neurolin, a cell surface glycoprotein on growing retinal axons in the goldfish visual system, is reexpressed during retinal axonal regeneration. J Cell Biol. 1992 May;117(4):863–875. doi: 10.1083/jcb.117.4.863. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Pollerberg G. E., Burridge K., Krebs K. E., Goodman S. R., Schachner M. The 180-kD component of the neural cell adhesion molecule N-CAM is involved in cell-cell contacts and cytoskeleton-membrane interactions. Cell Tissue Res. 1987 Oct;250(1):227–236. doi: 10.1007/BF00214676. [DOI] [PubMed] [Google Scholar]
  23. Pollerberg G. E., Mack T. G. 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. 1994 Oct;165(2):670–687. doi: 10.1006/dbio.1994.1284. [DOI] [PubMed] [Google Scholar]
  24. Rathjen F. G., Wolff J. M., Chang S., Bonhoeffer F., Raper J. A. Neurofascin: a novel chick cell-surface glycoprotein involved in neurite-neurite interactions. Cell. 1987 Dec 4;51(5):841–849. doi: 10.1016/0092-8674(87)90107-3. [DOI] [PubMed] [Google Scholar]
  25. Raymond P. A. Movement of retinal terminals in goldfish optic tectum predicted by analysis of neuronal proliferation. J Neurosci. 1986 Sep;6(9):2479–2488. doi: 10.1523/JNEUROSCI.06-09-02479.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Scholes J. H. Nerve fibre topography in the retinal projection to the tectum. Nature. 1979 Apr 12;278(5705):620–624. doi: 10.1038/278620a0. [DOI] [PubMed] [Google Scholar]
  27. Sretavan D. W., Reichardt L. F. Time-lapse video analysis of retinal ganglion cell axon pathfinding at the mammalian optic chiasm: growth cone guidance using intrinsic chiasm cues. Neuron. 1993 Apr;10(4):761–777. doi: 10.1016/0896-6273(93)90176-r. [DOI] [PubMed] [Google Scholar]
  28. 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. 1991 Feb;112(3):449–455. doi: 10.1083/jcb.112.3.449. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Stuermer C. A., Bastmeyer M., Bähr M., Strobel G., Paschke K. Trying to understand axonal regeneration in the CNS of fish. J Neurobiol. 1992 Jul;23(5):537–550. doi: 10.1002/neu.480230508. [DOI] [PubMed] [Google Scholar]
  30. Stuermer C. A., Easter S. S., Jr Rules of order in the retinotectal fascicles of goldfish. J Neurosci. 1984 Apr;4(4):1045–1051. doi: 10.1523/JNEUROSCI.04-04-01045.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Vielmetter J., Lottspeich F., Stuermer C. A. The monoclonal antibody E587 recognizes growing (new and regenerating) retinal axons in the goldfish retinotectal pathway. J Neurosci. 1991 Nov;11(11):3581–3593. doi: 10.1523/JNEUROSCI.11-11-03581.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Vielmetter J., Stolze B., Bonhoeffer F., Stuermer C. A. In vitro assay to test differential substrate affinities of growing axons and migratory cells. Exp Brain Res. 1990;81(2):283–287. doi: 10.1007/BF00228117. [DOI] [PubMed] [Google Scholar]
  33. Vielmetter J., Stuermer C. A. Goldfish retinal axons respond to position-specific properties of tectal cell membranes in vitro. Neuron. 1989 Apr;2(4):1331–1339. doi: 10.1016/0896-6273(89)90071-8. [DOI] [PubMed] [Google Scholar]
  34. Walsh C. Age-related fiber order in the ferret's optic nerve and optic chiasm. J Neurosci. 1986 Jun;6(6):1635–1642. doi: 10.1523/JNEUROSCI.06-06-01635.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Weikert T., Rathjen F. G., Layer P. G. Developmental maps of acetylcholinesterase and G4-antigen of the early chicken brain: long-distance tracts originate from AChE-producing cell bodies. J Neurobiol. 1990 Apr;21(3):482–498. doi: 10.1002/neu.480210309. [DOI] [PubMed] [Google Scholar]
  36. Wolburg H. Myelinated axons of ganglion cells in the retinae of teleosts. Cell Tissue Res. 1980;210(3):517–520. doi: 10.1007/BF00220207. [DOI] [PubMed] [Google Scholar]

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