Skip to main content
NCBI home page
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1992 May 2;117(4):863–875. doi: 10.1083/jcb.117.4.863

Neurolin, a cell surface glycoprotein on growing retinal axons in the goldfish visual system, is reexpressed during retinal axonal regeneration

PMCID: PMC2289455  PMID: 1577862

Abstract

The mAb E 21 recognizes a cell surface glycoprotein selectively associated with fish retinal ganglion cell axons that are in a state of growth. All retinal axons and ganglion cells in goldfish embryos stained for E 21. In adult fish, however, E 21 immunoreactivity exhibited a patterned distribution in ganglion cells in the marginal growth zone of the continuously enlarging fish retina and the new axons emerging from these cells in the retina, optic nerve, and optic tract. The E 21 antigen was absent from older axons, except the terminal arbor layer in the tectum, the Stratum fibrosum et griseum superficiale where it was uniformly distributed. Upon optic nerve transection, the previously unlabeled axons reacquired E 21 positivity as they regenerated throughout their path to the tectum. Several months after ONS, however, E 21 staining disappeared from the regenerated axons over most of their lengths but reappeared as in normal fish in the terminal arbor layer. The immunoaffinity-purified E 21 antigen, called Neurolin, has an apparent molecular mass of 86 kD and contains the HNK1/L2 carbohydrate moiety, like several members of the class of cell adhesion molecules of the Ig superfamily. The NH2-terminal amino acid sequence has homologies to the cell adhesion molecule DM-Grasp recently described in the chicken. Thus, retinal ganglion cell axons express Neurolin during their development and are able to reexpress this candidate cell adhesion molecule during axonal regeneration, suggesting that Neurolin is functionally important for fish retinal axon growth.

Full Text

The Full Text of this article is available as a PDF (5.0 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Anderson H. Adhesion molecules and animal development. Experientia. 1990 Jan 15;46(1):2–13. doi: 10.1007/BF01955407. [DOI] [PubMed] [Google Scholar]
  2. Bastiani M. J., Harrelson A. L., Snow P. M., Goodman C. S. Expression of fasciclin I and II glycoproteins on subsets of axon pathways during neuronal development in the grasshopper. Cell. 1987 Mar 13;48(5):745–755. doi: 10.1016/0092-8674(87)90072-9. [DOI] [PubMed] [Google Scholar]
  3. 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]
  4. Bieber A. J., Snow P. M., Hortsch M., Patel N. H., Jacobs J. R., Traquina Z. R., Schilling J., Goodman C. S. Drosophila neuroglian: a member of the immunoglobulin superfamily with extensive homology to the vertebrate neural adhesion molecule L1. Cell. 1989 Nov 3;59(3):447–460. doi: 10.1016/0092-8674(89)90029-9. [DOI] [PubMed] [Google Scholar]
  5. Bixby J. L., Zhang R. Purified N-cadherin is a potent substrate for the rapid induction of neurite outgrowth. J Cell Biol. 1990 Apr;110(4):1253–1260. doi: 10.1083/jcb.110.4.1253. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. 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]
  7. Chang S., Rathjen F. G., Raper J. A. Neurite outgrowth promoting activity of G4 and its inhibition by monoclonal antibodies. J Neurosci Res. 1990 Feb;25(2):180–186. doi: 10.1002/jnr.490250205. [DOI] [PubMed] [Google Scholar]
  8. Dodd J., Morton S. B., Karagogeos D., Yamamoto M., Jessell T. M. Spatial regulation of axonal glycoprotein expression on subsets of embryonic spinal neurons. Neuron. 1988 Apr;1(2):105–116. doi: 10.1016/0896-6273(88)90194-8. [DOI] [PubMed] [Google Scholar]
  9. Doherty P., Cohen J., Walsh F. S. Neurite outgrowth in response to transfected N-CAM changes during development and is modulated by polysialic acid. Neuron. 1990 Aug;5(2):209–219. doi: 10.1016/0896-6273(90)90310-c. [DOI] [PubMed] [Google Scholar]
  10. 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]
  11. 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]
  12. Easter S. S., Jr, Stuermer C. A. An evaluation of the hypothesis of shifting terminals in goldfish optic tectum. J Neurosci. 1984 Apr;4(4):1052–1063. doi: 10.1523/JNEUROSCI.04-04-01052.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Eckerskorn C., Mewes W., Goretzki H., Lottspeich F. A new siliconized-glass fiber as support for protein-chemical analysis of electroblotted proteins. Eur J Biochem. 1988 Oct 1;176(3):509–519. doi: 10.1111/j.1432-1033.1988.tb14308.x. [DOI] [PubMed] [Google Scholar]
  14. 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]
  15. Giordano S., Hall C., Quitschke W., Glasgow E., Schechter N. Keratin 8 of simple epithelia is expressed in glia of the goldfish nervous system. Differentiation. 1990 Sep;44(3):163–172. doi: 10.1111/j.1432-0436.1990.tb00614.x. [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. 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. 1991 May;112(1):51–67. doi: 10.1242/dev.112.1.51. [DOI] [PubMed] [Google Scholar]
  18. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  19. Lagenaur C., Lemmon V. An L1-like molecule, the 8D9 antigen, is a potent substrate for neurite extension. Proc Natl Acad Sci U S A. 1987 Nov;84(21):7753–7757. doi: 10.1073/pnas.84.21.7753. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Lanners H. N., Grafstein B. Early stages of axonal regeneration in the goldfish optic tract: an electron microscopic study. J Neurocytol. 1980 Dec;9(6):733–751. doi: 10.1007/BF01205016. [DOI] [PubMed] [Google Scholar]
  21. Martini R., Schachner M. Immunoelectron microscopic localization of neural cell adhesion molecules (L1, N-CAM, and myelin-associated glycoprotein) in regenerating adult mouse sciatic nerve. J Cell Biol. 1988 May;106(5):1735–1746. doi: 10.1083/jcb.106.5.1735. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Matsunaga M., Hatta K., Nagafuchi A., Takeichi M. Guidance of optic nerve fibres by N-cadherin adhesion molecules. Nature. 1988 Jul 7;334(6177):62–64. doi: 10.1038/334062a0. [DOI] [PubMed] [Google Scholar]
  23. Noronha A. B., Ilyas A., Antonicek H., Schachner M., Quarles R. H. Molecular specificity of L2 monoclonal antibodies that bind to carbohydrate determinants of neural cell adhesion molecules and their resemblance to other monoclonal antibodies recognizing the myelin-associated glycoprotein. Brain Res. 1986 Oct 22;385(2):237–244. doi: 10.1016/0006-8993(86)91069-3. [DOI] [PubMed] [Google Scholar]
  24. 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]
  25. Quitschke W., Schechter N. In vitro protein synthesis in the goldfish retinotectal pathway during regeneration: evidence for specific axonal proteins of retinal origin in the optic nerve. J Neurochem. 1983 Oct;41(4):1137–1142. doi: 10.1111/j.1471-4159.1983.tb09063.x. [DOI] [PubMed] [Google Scholar]
  26. Rabacchi S. A., Neve R. L., Dräger U. C. A positional marker for the dorsal embryonic retina is homologous to the high-affinity laminin receptor. Development. 1990 Jul;109(3):521–531. doi: 10.1242/dev.109.3.521. [DOI] [PubMed] [Google Scholar]
  27. 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]
  28. Rathjen F. G., Wolff J. M., Frank R., Bonhoeffer F., Rutishauser U. Membrane glycoproteins involved in neurite fasciculation. J Cell Biol. 1987 Feb;104(2):343–353. doi: 10.1083/jcb.104.2.343. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. 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]
  30. Reh T. A., Constantine-Paton M. Retinal ganglion cell terminals change their projection sites during larval development of Rana pipiens. J Neurosci. 1984 Feb;4(2):442–457. doi: 10.1523/JNEUROSCI.04-02-00442.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Skene J. H. Axonal growth-associated proteins. Annu Rev Neurosci. 1989;12:127–156. doi: 10.1146/annurev.ne.12.030189.001015. [DOI] [PubMed] [Google Scholar]
  32. Springer A. D., Gaffney J. S. Retinal projections in the goldfish: a study using cobaltous-lysine. J Comp Neurol. 1981 Dec 10;203(3):401–424. doi: 10.1002/cne.902030306. [DOI] [PubMed] [Google Scholar]
  33. Stuermer C. A., Easter S. S., Jr A comparison of the normal and regenerated retinotectal pathways of goldfish. J Comp Neurol. 1984 Feb 10;223(1):57–76. doi: 10.1002/cne.902230106. [DOI] [PubMed] [Google Scholar]
  34. 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]
  35. Stuermer C. A., Raymond P. A. Developing retinotectal projection in larval goldfish. J Comp Neurol. 1989 Mar 22;281(4):630–640. doi: 10.1002/cne.902810411. [DOI] [PubMed] [Google Scholar]
  36. Stuermer C. A. Rules for retinotectal terminal arborizations in the goldfish optic tectum: a whole-mount study. J Comp Neurol. 1984 Oct 20;229(2):214–232. doi: 10.1002/cne.902290207. [DOI] [PubMed] [Google Scholar]
  37. Stuermer C. A. Trajectories of regenerating retinal axons in the goldfish tectum: II. Exploratory branches and growth cones on axons at early regeneration stages. J Comp Neurol. 1988 Jan 1;267(1):69–91. doi: 10.1002/cne.902670106. [DOI] [PubMed] [Google Scholar]
  38. 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. 1991 Oct;7(4):535–545. doi: 10.1016/0896-6273(91)90366-8. [DOI] [PubMed] [Google Scholar]
  39. Tesser P., Jones P. S., Schechter N. Elevated levels of retinal neurofilament mRNA accompany optic nerve regeneration. J Neurochem. 1986 Oct;47(4):1235–1243. doi: 10.1111/j.1471-4159.1986.tb00745.x. [DOI] [PubMed] [Google Scholar]
  40. Towbin H., Staehelin T., Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350–4354. doi: 10.1073/pnas.76.9.4350. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. 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]
  42. 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]

Articles from The Journal of Cell Biology are provided here courtesy of The Rockefeller University Press

RESOURCES