Skip to main content
Log in

Expression of the dm-20 isoform of the plp gene in olfactory nerve ensheathing cells: evidence from developmental studies

  • Published:
Journal of Neurocytology

Abstract

The olfactory bulb is a specialized area of the CNS with well-defined areas containing both myelinated, and non-myelinated axons. The presence of plp gene transcripts has been demonstrated previously in the olfactory bulb, but no detailed description of plp gene activity in this complex area of the CNS is available. In this study we describe the developmental expression of the two plp gene isoforms, plp and dm-20, and their products in the mouse olfactory bulb. plp gene activity was present in the non-myelinated olfactory nerve layer of the bulb from E14 through to adult ages. Expression in the deeper layers of the bulb, associated with myelination of the second order axons, was apparent from P10 onwards. dm-20 was the predominant isoform expressed at the transcript level in the olfactory nerve layer and was the only isoprotein demonstrable by immunostaining. This expression was associated with the resident glial cell of the non-myelinated olfactory nerve layer, the olfactory nerve ensheathing cell. Selective expression of the DM-20 isoprotein in the non-myelin forming olfactory nerve ensheathing cells implies a role for DM-20 other than as a structural myelin protein. Further study of this specialized glial cell may prove useful in elucidating the specific function(s) of the DM-20 isoprotein.

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

  • BARNETT, S. C., HUTCHINS, A. M. & NOBLE, M. (1993) Purification of olfactory nerve ensheathing cells from the olfactory bulb. Developmental Biology 155, 337–50.

    Google Scholar 

  • CAMPAGNONI, C. W., GARBAY, B., MICEVYCH, P., PRIBYL, T., KAMPF, K., HANDLEY, V. W. & CAMPAGNONI, A. T. (1992) DM20 mRNA splice product of the myelin proteolipid protein gene is expressed in the murine heart. Journal of Neuroscience Research 33, 148–55.

    Google Scholar 

  • DE LORENZO, A. J. (1957) Electron microscopic observations of the olfactory mucosa and olfactory nerve. Journal of Biophysical and Biochemical Cytology 3, 839–48.

    Google Scholar 

  • DEVON, R. & DOUCETTE, R. (1992) Olfactory ensheathing cells myelinate dorsal root ganglion neurites. Brain Research 589, 175–9.

    Google Scholar 

  • DICKINSON, P. J., FANARRAGA, M. L., GRIFFITHS, I. R., BARRIE, J. M., KYRIAKIDES, E., MONTAGUE, P. (1996) Oligodendrocyte progenitors in the embryonic spinal cord express DM-20. Neuropathology and Applied Neurobiology 22, 188–98.

    Google Scholar 

  • DOUCETTE, J. R. (1984) The glial cells in the nerve fiber layer of the rat olfactory bulb. Anatomical Record 210, 385–91.

    Google Scholar 

  • DOUCETTE, R. (1989) Development of the nerve fiber layer in the olfactory bulb of mouse embryos. Journal of Comparative Neurology 285, 514–27.

    Google Scholar 

  • DOUCETTE, R. (1990) Glial influences on axonal growth in the primary olfactory system. Glia 3, 433–49.

    Google Scholar 

  • DUBOIS-DALCQ, M., BEHAR, T., HUDSON, L. D. & LAZZARINI, R. A. (1986) Emergence of three myelin proteins in oligodendrocytes cultured without neurons. Journal of Cell Biology 102, 384–92.

    Google Scholar 

  • EINSENBARTH, G. S., WALSH, F. S. & NIRENBERG, M. (1979) Monoclonal antibody to a plasma membrane antigen of neurons. Proceedings of the National Academy of Sciences (USA) 76, 4913–17.

    Google Scholar 

  • FANARRAGA, M., SOMMER, I., GRIFFITHS, I. R., MONTAGUE, P., GROOME, N. P., NAVE, K., SCHNEIDER, A., BROPHY, P. J. & KENNEDY, P. G. E. (1993) Oligodendrocyte development and differentiation in the rumpshaker mutation. Glia 9, 146–56.

    Google Scholar 

  • FRANCESCHINI, I. A. & BARNETT, S. C. (1996) Low affinity NGF receptor and E-N-CAM expression defines two types of olfactory nerve ensheathing cells that share a common lineage. Developmental Biology 173, 327–43.

    Google Scholar 

  • FRANKLIN, R. J. M., GILSON, J. M., FRANCESCHINI, I. A. & BARNETT, S. C. (1996) Schwann cell-like myelination following transplantation of an olfactory bulb-ensheathing cell line into areas of demyelination in the adult CNS. Glia 17, 217–24.

    Google Scholar 

  • GASSER, H. S. (1956) Olfactory nerve fibres. Journal of General Physiology 39, 473–96.

    Google Scholar 

  • GOW, A., FRIEDRICH, V. L., JR & LAZZARINI, R. A. (1994) Intracellular transport and sorting of the oligodendrocyte transmembrane proteolipid protein. Journal of Neuroscience Research 37, 563–73.

    Google Scholar 

  • GRAZIADEI, P. P. C. & MONTI GRAZIADEI, G. A. (1979) Neurogenesis and neuron regeneration in the olfactory system of mammals. I. Morphological aspects of differentiation and structural organization of the olfactory sensory neurones. Journal of Neurocytology 8, 1–18.

    Google Scholar 

  • GRIFFITHS, I. R., MITCHELL, L. S., MCPHILEMY, K., MORRISON, S., KYRIAKIDES, E. & BARRIE, J. A. (1989) Expression of myelin protein genes in Schwann cells. Journal of Neurocytology 18, 345–52.

    Google Scholar 

  • GRIFFITHS, I. R., DICKINSON, P. & MONTAGUE, P. (1995) Expression of the proteolipid protein gene in glial cells of the post natal peripheral nervous system of rodents. Neuropathology and Applied Neurobiology 21, 97–110.

    Google Scholar 

  • IKENAKA, K., KAGAWA, T. & MIKOSHIBA, K. (1992) Selective expression of DM-20, an alternatively spliced myelin proteolipid protein gene product, in developing nervous system and in non-glial cells. Journal of Neurochemistry 58, 2248–53.

    Google Scholar 

  • JACOBSON, S. (1963) Sequence of myelination in the brain of the albino rat. Journal of Comparative Neurology 121, 5–29.

    Google Scholar 

  • KANFER, J., PARENTY, M., GOUJET-ZALC, C., MONGE, M., BERNIER, L., CAMPAGNONI, A. T., DAUTIGNY, A. & ZALC, B. (1989) Developmental expression of myelin proteolipid, basic protein and 2′, 3′-cyclic nucleotide 3′-phosphodiesterase transcripts in different rat brain regions. Journal of Molecular Neuroscience 1, 39–46.

    Google Scholar 

  • KITAGAWA, K., SINOWAY, M. P., YANG, C., GOULD, R. M. & COLMAN, D. R. (1993) A proteolipid protein gene family: expression in sharks and rays and possible evolution from an ancestral gene encoding a pore-forming polypeptide. Neuron 11, 433–48.

    Google Scholar 

  • KRONQUIST, K. E., CRANDALL, B. F., MACKLIN, W. B., CAMPAGNONI, A. T. (1987) Expression of myelin proteins in the developing human spinal cord: cloning and sequencing of human proteolipid protein cDNA. Journal of Neuroscience Research 18, 395–401.

    Google Scholar 

  • LEVINE, S. M., WONG, D. & MACKLIN, W. B. (1990) Developmental expression of proteolipid protein and DM20 mRNAs and proteins in the rat brain. Developmental Neuroscience 12, 235–50.

    Google Scholar 

  • MITCHELL, L. S., GILLESPIE, C. S., MCALLISTER, F., FANARRAGA, M., KIRKHAM, D., KELLY, B., BROPHY, P. J., GRIFFITHS, I. R., MONTAGUE, P. & KENNEDY, P. G. E. (1992) Developmental expression of the major myelin protein genes in the CNS of the X-linked hypomyelinating mutant rumpshaker. Journal of Neuroscience Research 33, 205–17.

    Google Scholar 

  • NADON, N. L., DUNCAN, I. D. & HUDSON, L. D. (1990) A point mutation in the proteolipid protein gene of the 'shaking pup’ interrupts oligodendrocyte development. Development 110, 529–37.

    Google Scholar 

  • NAVE, K., LAI, C., BLOOM, F. E. & MILNER, R. J. (1987) Splice site selection in the proteolipid protein (PLP) gene transcript and primary structure of the DM-20 protein of central nervous system myelin. Proceedings of the National Academy of Sciences (USA) 84, 5665–9.

    Google Scholar 

  • NAVE, K., SCHNEIDER, A., READHEAD, C., GRIFFITHS, I. R., PÜHLHOFER, A., BARTHOLOMÄ, A., GRAF, S. & KIEFER, B. (1994) Molecular biology and neurogenetics of myelin proteolipid protein. In A Multidisciplinary Approach to Myelin Diseases II (edited by SALVATI, S.) pp. 115–26. New York: Plenum Press.

    Google Scholar 

  • NORGREN, R. B., RATNER, N. & BRACKENBURY, R. (1992) Development of olfactory nerve glia defined by a monoclonal antibody specific for Schwann cells. Developmental Dynamics 194, 231–8.

    Google Scholar 

  • PHAM-DINH, D., BIRLING, M., DAUTIGNY, A. & NUSSBAUM, J. L. (1991) Proteolipid DM-20 predominates over PLP in peripheral nervous system. Molecular Neuroscience 2, 89–92.

    Google Scholar 

  • PHILPOT, B. D., KLINTSOVA, A. Y. & BRUNJES, P. C. (1995) Oligodendrocyte/myelin-immunoreactivity in the developing olfactory system. Neuroscience 67, 1009–19.

    Google Scholar 

  • PUCKETT, C., HUDSON, L. D., ONO, K., BENECKE, J., DUBOIS-DALCQ, M. & LAZZARINI, R. A. (1987) Myelin-specific proteolipid protein is expressed in myelinating Schwann cells but is not incorporated into myelin sheaths. Journal of Neuroscience Research 18, 511–18.

    Google Scholar 

  • RAFF, M. C., MILLER, R. H. & NOBLE, M. (1983) A glial progenitor that develops in vitro into an astrocyte or an oligodendrocyte depending on culture medium. Nature 303, 390–6.

    Google Scholar 

  • SCHNEIDER, A., MONTAGUE, P., GRIFFITHS, I. R., FANARRAGA, M., KENNEDY, P. G. E., BROPHY, P. J. & NAVE, K. (1992) Uncoupling of hypomyelination and glial cell death by a mutation in the proteolipid protein gene. Nature 358, 758–61.

    Google Scholar 

  • SHIOTA, C., MIURA, M. & MIKOSHIBA, K. (1989) Developmental profile and differential localization of mRNAs of myelin proteins (MBP and PLP) in oligodendrocytes in the brain and in culture. Developmental Brain Research 45, 83–94.

    Google Scholar 

  • SOMMER, I. & SCHACHNER, M. (1981) Monoclonal antibodies (O1-O4) to oligodendrocyte cell surfaces: an immunocytological study in the central nervous system. Developmental Biology 83, 311–27.

    Google Scholar 

  • SOMMER, I. & SCHACHNER, M. (1984) Stage-specific antigens on oligodendrocyte cell surfaces. In The Role of Cell Interactions in Early Neurogenesis (edited by DUPRET, A-M., KATO, A. C. & WEBER, M.) pp. 201–5. New York: Plenum Press.

    Google Scholar 

  • TILNEY, F. (1933) Behaviour in its relation to development of the brain: correlation between development of brain and behaviour in the albino rat from embryonic states to maturity. Bulletin of the Neurological Institute N.Y. 3, 252–358.

    Google Scholar 

  • TIMSIT, S. G., BALLY-CUIF, L., COLMAN, D. R. & ZALC, B. (1992) DM-20 mRNA is expressed during the embryonic development of the nervous system of the mouse. Journal of Neurochemistry 58, 1172–5.

    Google Scholar 

  • TIMSIT, S., MARTINEZ, S., ALLINQUANT, B., PEYRON, F., PUELLES, L. & ZALC, B. (1995) Oligodendrocytes originate in a restricted zone of the embryonic ventral neural tube defined by DM-20 mRNA expression. Journal of Neuroscience 15, 1012–24.

    Google Scholar 

  • VALVERDE, F. & LOPEZ-MASCARAQUE, L. (1991) Neuroglial arrangements in the olfactory glomeruli of the hedgehog. Journal of Comparative Neurology 307, 658–74.

    Google Scholar 

  • VALVERDE, F., SANTACANA, M. & HEREDIA, M. (1992) Formation of an olfactory glomerulus: morphological aspects of development and organization. Neuroscience 49, 255–75.

    Google Scholar 

  • VAN DORSSELAER, A., NEBHL, R., SOROKINE, O., SCHINDLER, P. & LUU, B. (1987) The DM-20 proteolipid is a major brain protein. It is synthesised earlier in foetal life than the major myelin proteolipid (PLP). Compte Rendu Academy Science Paris 305, 555–60.

    Google Scholar 

  • WIGHT, P. A., DUCHALA, C. S., READHEAD, C. & MACKLIN, W. B. (1993) A myelin proteolipid protein-LacZ fusion protein is developmentally regulated and targeted to the myelin membrane in transgenic mice. Journal of Cell Biology 123, 443–54.

    Google Scholar 

  • YU, W.-P., COLLARINI, E. J., PRINGLE, N. P. & RICHARDSON, W. D. (1994) Embryonic expression of myelin genes: evidence for a focal source of oligodendrocyte precursors in the ventricular zone of the neural tube. Neuron 12, 1353–62.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Dickinson, P.J., Griffiths, I.R., Barrie, J.M. et al. Expression of the dm-20 isoform of the plp gene in olfactory nerve ensheathing cells: evidence from developmental studies. J Neurocytol 26, 181–189 (1997). https://doi.org/10.1023/A:1018584013739

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1018584013739

Keywords

Navigation