Skip to main content
Log in

Genes encoding giant danio and golden shiner ependymin

  • Original Articles
  • Published:
Neurochemical Research Aims and scope Submit manuscript

Abstract

Ependymin (EPN) is a brain glycoprotein that functions as a neurotrophic factor in optic nerve regeneration and long-term memory consolidation in goldfish. To date, trueepn genes have been characterized in one order of teleost fish,Cypriniformes. In the study presented here, polymerase chain reactions were used to analyze the completeepn genes,gd (1480 bp), andsh (2071 bp), fromCypriniformes giant danio and shiner, respectively. Southern hybridizations demonstrated the existence of one copy of each gene per corresponding haploid, genome. Each gene was found to contain six exons and five introns. Genegd encodes a predicted 218-amino acid (aa) protein GD 93% conserved to goldfish EPN, whilesh encodes a predicted 214-aa protein SH 91% homologous to goldfish. Evidence is presented classifying proteins previously termed “EPNs” into two major categories: true EPNs and non-EPN cerebrospinal fluid glycoproteins. Proteins GD and SH contain all the hallmark features of true EPNs.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Adams, D. S., and Shashoua, V. E. 1994. Cloning and sequencing the genes encoding goldfish and carp ependymin. Gene 141:237–241.

    Article  PubMed  CAS  Google Scholar 

  2. Anderson, M. J., Choy, C. Y. and Waxman, S. G. 1986. Selforganization of ependyma in regenerating teleost spinal cord: Evidence from serial section reconstructions. J. Embryol. Exp. Morph. 96:1–18.

    PubMed  CAS  Google Scholar 

  3. Benowitz, L. I. and Shashoua, V. E. 1977. Localization of a brain protein metabolically linked with behavioral plasticity in the goldfish. Brain Res. 136:227–242.

    Article  PubMed  CAS  Google Scholar 

  4. Breathnach, R. and Chambon, P. 1981. Organization and expression of eukaryotic split genes coding for proteins. Ann. Rev. Biochem. 50:349–383.

    Article  PubMed  CAS  Google Scholar 

  5. Chernoff, E. A. G. 1994. Cutting the cord: Ependymal cells in spinal cord regeneration. Am. Zoologist 34(5):8aa.

    Google Scholar 

  6. Chernoff, E. A. G., and Stocum, D. L. 1995. Developmental aspacts of spinal cord and limb regeneration. Dev. Growth Diff. 37: 133–147.

    Article  Google Scholar 

  7. Doherty, P., Williams, E., and Walsh, F. S. 1995. A soluble chimeric form of the L1 glycoprotein stimulates neurite outgrowth. Neuron 14:57–66.

    Article  PubMed  CAS  Google Scholar 

  8. Egar, M., Simpson, S. B., and Singer, M. 1970. The growth and differentiation of the regenerating spinal cord of the lizard,Anolis carolinensis. J. Morphol. 131:131–152.

    Article  PubMed  CAS  Google Scholar 

  9. Egar, M., and Singer, M. 1972. The role of ependyma in spinal cord regeneration in the urodele,Triturus. Exp. Neurol. 37:422–430.

    Article  PubMed  CAS  Google Scholar 

  10. Ganss, B. and Hoffmann, W. 1993. Calcium binding to sialic acids and its effect of the conformation of ependymins. Eur. J. Biochem. 217:275–280.

    Article  PubMed  CAS  Google Scholar 

  11. Königstorfer, A., Sterrer, S., Eckerskorn, C., Lottspeich, F., Schmidt, R., and Hoffmann, W. 1989a. Molecular characterization of an ependymin precursor from goldfish brain. J. Neurochem. 52: 310–312.

    Article  PubMed  Google Scholar 

  12. Königstorfer, A., Sterrer, S. and Hoffmann, W. 1989b. Biosynthesis of ependymins from goldfish brain. J. Biol. Chem. 264: 13689–13692.

    PubMed  Google Scholar 

  13. Kruse, J., Mailhammer, R., Wernecke, H., Faissner, A., Sommer, I., Goridis, C., and Schachner, M. 1984. Neural cell adhesion molecules and myelin-associated glycoprotein share a common carbohydrate moiety recognized by monoclonal antibodies L2 and HNK-1. Nature 311:153–155.

    Article  PubMed  CAS  Google Scholar 

  14. Kyte, J. and Doolittle, R.F. 1982. A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 157:105–132.

    Article  PubMed  CAS  Google Scholar 

  15. Marshall, R. D. 1974. The nature and metabolism of the carbohydrate-peptide linkages of glycoproteins. Biochem. Soc. Symp. 40:17–26.

    PubMed  CAS  Google Scholar 

  16. Müller-Schmid, A., Rinder, H., Lottspeich, F., Gertzen, E. M. and Hoffmann, W. 1992. Ependymins from the cerebrospinal fluid of salmonid fish: gene structure and molecular characterization. Gene 118:189–196.

    Article  PubMed  Google Scholar 

  17. Müller-Schmid, A., Ganss, B., Gorr, T., and Hoffmann, W. 1993. Molecular analysis of ependymins from the cerebrospinal fluid of the orders Clupeiformes and Salmoniformes: No indication for the existence of an Euteleost infradivision. J. Mol. Evol. 36:578–585.

    Article  PubMed  Google Scholar 

  18. O'Hara, C. M., Egar, M. W., and Chernoff, E. A. G. 1992. Reorganization of the ependyma during axolotl spinal cord regeneration: Changes in intermediate filament and fibronectin expression. Dev. Dynamics 193:103–115.

    Google Scholar 

  19. Proudfoot, N. J. 1989. How RNA polymerase II terminates transcription in higher eukaryotes. Trends Biochem. Sci. 14:105–110.

    Article  PubMed  CAS  Google Scholar 

  20. Rinder, H., Bayer, T. A., Gertzen, E. M., and Hoffmann, W. 1992. Molecular analysis of the ependymin gene and functional test of its promoter region by transient expression inBrachydanio rerio. DNA and Cell Biol. 11:425–432.

    Article  CAS  Google Scholar 

  21. Sanger, F., Nicklen, S. and Coulson, A. R. 1977. DNA sequencing with chain terminating inhibitors. Proc. Natl. Acad. Sci. USA 71: 5463–5467.

    Article  Google Scholar 

  22. Schmidt, R. 1986. Biochemical participation of glycoproteins in memory consolidation after two different training paradigms in goldfish. Adv. Biosci. 59:213–222.

    CAS  Google Scholar 

  23. Schmidt, J. T. and Shashoua, V. E. 1988. Antibodies to ependymin block the sharpening of the regenerating retinotectal projection in goldfish. Brain Res. 446:269–284.

    Article  PubMed  CAS  Google Scholar 

  24. Schmidt, R., Rother, S., Schlingensiepen, K., and Brysch, W. 1992. Neuronal plasticity depending on a glycoprotein synthesized in goldfish leptomeninx. Prog. Brain Res. 91:7–12.

    Article  PubMed  CAS  Google Scholar 

  25. Seidah, N. G., Day, R., Marcinkiewicz, M., Benjannet, S., and Chretien, M. 1991. Mammalian neural and endocrine pro-protein and pro-hormone convertases belonging to the sutilisin family of serine proteinases. Enzyme 45:271–284.

    PubMed  CAS  Google Scholar 

  26. Shashoua, V. E. 1976. Brain metabolism and the acquisition of new behaviors, I. Evidence for specific changes in the pattern of protein synthesis. Brain Res. 111:347–364.

    Article  PubMed  CAS  Google Scholar 

  27. Shashoua, V. E. 1981. Extracellular fluid proteins of goldfish brain: studies on concentration and labeling patterns. Neurochem. Res. 6:1129–1147.

    Article  PubMed  CAS  Google Scholar 

  28. Shashoua, V. E. 1985. The role of brain extracellular proteins in neuroplasticity and learning. Cell. Molec. Neurobiol. 5:183–207.

    Article  PubMed  CAS  Google Scholar 

  29. Shashoua, V. E. 1986. The role of neurosecretory cells in learning and memory. Adv. Biosci. 61:245–254.

    CAS  Google Scholar 

  30. Shashoua, V. E. 1988. Monomeric and polymeric forms of ependymin: A brain extracellular glycoprotein implicated in memory consolidation processes. Neurochem. Res. 13:649–655.

    Article  PubMed  CAS  Google Scholar 

  31. Shashoua, V. E. 1991. Ependymin, a brain extracellular glycoprotein, and CNS plasticity. Annals NY Acad. Sci. 627:94–114.

    CAS  Google Scholar 

  32. Shashoua, V. E., and Moore, M. E. 1978. Effect of antisera to β and goldfish brain proteins on the retention of newly acquired behavior. Brain Res. 148:441–449.

    Article  PubMed  CAS  Google Scholar 

  33. Shashoua, V. E., Daniel, P. F., Moore, M. E., and Jungalwala, F. B. 1986. Demonstration of glucuronic acid on brain glycoproteins which react with HNK-1 antibody. Biochem. Biophys. Res. Commun. 138:902–909.

    Article  PubMed  CAS  Google Scholar 

  34. Shashoua, V. E., and Hesse, G. W. 1989. Classical conditioning leads to changes in extracellular concentrations of ependymin in goldfish brain. Brain Res. 484:333–339.

    Article  PubMed  CAS  Google Scholar 

  35. Shashoua, V. E., Nolan, P. M., and Milinazzo, B. 1991. Ependymin promotes neurite growth in neuroblastoma cell cultures. Soc. Neurosci. Abst. 17:95, 12.

    Google Scholar 

  36. Simpson, S. B. Jr. 1968. Morphology of the regenerated spinal cord in the lizard,Anolis carolinensis. J. Comp. Neurol. 134:193–210.

    Article  PubMed  Google Scholar 

  37. Singer, M., Nordlander, R. H., and Egar, M. 1979. Axonal guidance during embryogenesis and regeneration in the spinal cord of newt: The blueprint hypothesis of neuronal pathway patterning. J. Comp. Neurol. 185:1–22.

    Article  PubMed  CAS  Google Scholar 

  38. Sterrer, S., Königstorfer, A., and Hoffmann, W. 1990. Biosynthesis and expression of ependymin homologous sequences in zebrafish brain. Neuroscience 37:277–284.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to David S. Adams.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Adams, D.S., Kiyokawa, M., Getman, M.E. et al. Genes encoding giant danio and golden shiner ependymin. Neurochem Res 21, 377–384 (1996). https://doi.org/10.1007/BF02531655

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02531655

Key words

Navigation