Neurochemical Research

, Volume 21, Issue 3, pp 377–384 | Cite as

Genes encoding giant danio and golden shiner ependymin

  • David S. Adams
  • Miki Kiyokawa
  • Michael E. Getman
  • Victor E. Shashoua
Original Articles

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.

Key words

Ependymin neurotrophic factor Danio aequipinnatus Notropis chrysoleucas 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Adams, D. S., and Shashoua, V. E. 1994. Cloning and sequencing the genes encoding goldfish and carp ependymin. Gene 141:237–241.PubMedCrossRefGoogle Scholar
  2. 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.PubMedGoogle Scholar
  3. 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.PubMedCrossRefGoogle Scholar
  4. 4.
    Breathnach, R. and Chambon, P. 1981. Organization and expression of eukaryotic split genes coding for proteins. Ann. Rev. Biochem. 50:349–383.PubMedCrossRefGoogle Scholar
  5. 5.
    Chernoff, E. A. G. 1994. Cutting the cord: Ependymal cells in spinal cord regeneration. Am. Zoologist 34(5):8aa.Google Scholar
  6. 6.
    Chernoff, E. A. G., and Stocum, D. L. 1995. Developmental aspacts of spinal cord and limb regeneration. Dev. Growth Diff. 37: 133–147.CrossRefGoogle Scholar
  7. 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.PubMedCrossRefGoogle Scholar
  8. 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.PubMedCrossRefGoogle Scholar
  9. 9.
    Egar, M., and Singer, M. 1972. The role of ependyma in spinal cord regeneration in the urodele,Triturus. Exp. Neurol. 37:422–430.PubMedCrossRefGoogle Scholar
  10. 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.PubMedCrossRefGoogle Scholar
  11. 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.PubMedCrossRefGoogle Scholar
  12. 12.
    Königstorfer, A., Sterrer, S. and Hoffmann, W. 1989b. Biosynthesis of ependymins from goldfish brain. J. Biol. Chem. 264: 13689–13692.PubMedGoogle Scholar
  13. 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.PubMedCrossRefGoogle Scholar
  14. 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.PubMedCrossRefGoogle Scholar
  15. 15.
    Marshall, R. D. 1974. The nature and metabolism of the carbohydrate-peptide linkages of glycoproteins. Biochem. Soc. Symp. 40:17–26.PubMedGoogle Scholar
  16. 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.PubMedCrossRefGoogle Scholar
  17. 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.PubMedCrossRefGoogle Scholar
  18. 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. 19.
    Proudfoot, N. J. 1989. How RNA polymerase II terminates transcription in higher eukaryotes. Trends Biochem. Sci. 14:105–110.PubMedCrossRefGoogle Scholar
  20. 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.CrossRefGoogle Scholar
  21. 21.
    Sanger, F., Nicklen, S. and Coulson, A. R. 1977. DNA sequencing with chain terminating inhibitors. Proc. Natl. Acad. Sci. USA 71: 5463–5467.CrossRefGoogle Scholar
  22. 22.
    Schmidt, R. 1986. Biochemical participation of glycoproteins in memory consolidation after two different training paradigms in goldfish. Adv. Biosci. 59:213–222.Google Scholar
  23. 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.PubMedCrossRefGoogle Scholar
  24. 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.PubMedCrossRefGoogle Scholar
  25. 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.PubMedGoogle Scholar
  26. 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.PubMedCrossRefGoogle Scholar
  27. 27.
    Shashoua, V. E. 1981. Extracellular fluid proteins of goldfish brain: studies on concentration and labeling patterns. Neurochem. Res. 6:1129–1147.PubMedCrossRefGoogle Scholar
  28. 28.
    Shashoua, V. E. 1985. The role of brain extracellular proteins in neuroplasticity and learning. Cell. Molec. Neurobiol. 5:183–207.PubMedCrossRefGoogle Scholar
  29. 29.
    Shashoua, V. E. 1986. The role of neurosecretory cells in learning and memory. Adv. Biosci. 61:245–254.Google Scholar
  30. 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.PubMedCrossRefGoogle Scholar
  31. 31.
    Shashoua, V. E. 1991. Ependymin, a brain extracellular glycoprotein, and CNS plasticity. Annals NY Acad. Sci. 627:94–114.Google Scholar
  32. 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.PubMedCrossRefGoogle Scholar
  33. 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.PubMedCrossRefGoogle Scholar
  34. 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.PubMedCrossRefGoogle Scholar
  35. 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. 36.
    Simpson, S. B. Jr. 1968. Morphology of the regenerated spinal cord in the lizard,Anolis carolinensis. J. Comp. Neurol. 134:193–210.PubMedCrossRefGoogle Scholar
  37. 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.PubMedCrossRefGoogle Scholar
  38. 38.
    Sterrer, S., Königstorfer, A., and Hoffmann, W. 1990. Biosynthesis and expression of ependymin homologous sequences in zebrafish brain. Neuroscience 37:277–284.PubMedCrossRefGoogle Scholar

Copyright information

© Plenum Publishing Corporation 1996

Authors and Affiliations

  • David S. Adams
    • 1
  • Miki Kiyokawa
    • 1
  • Michael E. Getman
    • 1
  • Victor E. Shashoua
    • 2
  1. 1.Department of Biology and BiotechnologyWorcester Polytechnic InstituteWorcesterUSA
  2. 2.Neuromedica, Inc.CambridgeUSA

Personalised recommendations