Skip to main content

CNS Myelination: What can we learn from phylogeny?

  • Conference paper
Molecular Signaling and Regulation in Glial Cells

Abstract

The morphology of embryonic and adult spiny dogfish and clearnose skate spinal cords were compared with rat. Myelination occurred in a nearly identical fashion in all three specimens. For example, oligodendrocytes appear first in the ventricle funiculus (vf), coordinate with the development of large (one micron diameter) axons. Since developing dogfish and skate neural cells express the same cell-type-specific antigens, immunofluorescence was used to study their spatial and temporal appearance. In all cases, the order of appearance was: radial glia (GFAP+), neuronal perikaiya (P (non-phosphoiylated) neurofilament), axons (P+ neurofilament) and oligodendrocytes (04+, R-mAb+, 01+, MBP+, P0/PLP+).The morphological and biochemical similarities demonstrate that many features of myelination are conserved in these divergent lineages. Thus, differences between them, which include: lack of tight junctions (chondrichthye myelin), replacement of the P0 isoforms in fish with PLP in mammals, lack of exon 2-containing MBP isoforms, myelin-associated glycoprotein (MAG), myelin oligodendrocyte protein (MOG), CNPase and MBP mRNA translocation (chondrichthye), are all derived features; differences do not alter myelin function. Preliminary evidence suggests that myelinating oligodendrocytes are related to glial cells that ensheath, but do not myelinate, large caliber axons in lamprey spinal cord. MBP-like molecules are detected in lamprey spinal cord by RT-PCR (reverse transcriptase-polymerase chain reaction). Furthermore, polyclonal antibodies to mammalian and shark MBP recognize antigens expressed by lamprey spinal cord glial cells. We conclude that the understanding of human myelination will be enriched through comparative studies of vertebrates that lack (lamprey and hagfish) and display (non-mammalian vertebrates) myelination.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Arifins Kappers, C. U., G. C. Huber, and E. C. Crosby. (1936) The Comparative Anatomy of the Nervous System of Vertebrates Including Man. MacMillan, New York.

    Google Scholar 

  2. Bhattacharyya, A., E. Frank, N. Ratner, and R. Brackenbury. (1991) P0 is an early marker of the Schwann cell lineage in chickens. Neuron 7:831 –844.

    Article  PubMed  CAS  Google Scholar 

  3. Breitschopf, H., G. Suchanek, R. M. Gould, D. R. Colman, and H. Lassmann. (1992) In situ hybridization with digoxigenin-labeled probes: sensitive and reliable detection method applied to myelinating rat brain. Acta Neuropathol. (Berl.) 84:581–587.

    Article  CAS  Google Scholar 

  4. Chapman, E. R. and R. Jahn. (1994) Calcium-dependent interaction of the cytoplasmic region of synaptotagmin with membranes. J. Biol. Chem. 269:5735–5741.

    PubMed  CAS  Google Scholar 

  5. Clark, J. D., L.-L. Lin, R. W. Kriz, C. S. Ramesha, L. A. Sultzman, A. Lin, Y., N. Milona, and J. L. Knopf. (1991) A novel arachidonic acid-selective cytosolic PLA2 contains a Ca2+-dependent translocation domain with homology to PKC and GAP. Cell 65:1043–1051.

    Article  PubMed  CAS  Google Scholar 

  6. Hardy, R. and R Reynolds. (1991) Proliferation and differentiation potential of rat forebrain oligodendroglial progenitors both in vitro and in vivo. Development 111:1061–1080.

    PubMed  CAS  Google Scholar 

  7. Ikenaka, K., T. Kagawa, and K. Mikoshiba. (1992) Selective expression of DM-20, an alternatively spliced myelin proteolipid protein gene product, in developing nervous system and in nonglial cells. J. Neurochem. 58:2248–2253.

    Article  PubMed  CAS  Google Scholar 

  8. Jeserich, G. and T. V. Waehneldt. (1986) Bony fish myelin: evidence for common major structural glycoproteins in central and peripheral myelin of trout. J. Neurochem. 46:525–533.

    Article  PubMed  CAS  Google Scholar 

  9. Johnson, G. D., R. S. Davidson, K. C. McNamee, G. Russell, D. Goodwin, and E. J. Holborow. (1982) Fading of immunofluorescence during microscopy: a study of the phenomenon and its remedy. J. Immunol. Methods 55:231 –242.

    Article  PubMed  CAS  Google Scholar 

  10. Kemali, M., E. Sada, A. Miralto, and G. Zummo. (1983) Central myelin in the shark Scyllium stellare (Elasmobranchii, Selachii).Zeit. Mikrosk. Anat. Forsch.,Leipzig 97:3–14.

    CAS  Google Scholar 

  11. Kirschner, D.A. and A.E. Blaurock. (1992) Organization, phylogenetic variation, and dynamic transitions of myelin. In R.E. Martenson, (ed) Myelin: Biology and Chemistry. CRC Press, Boca Raton, FL. 3–78.

    Google Scholar 

  12. Kitagawa, K., M. P. Sinoway, C. Yang, R. M. Gould, and D. R. Colman. (1993) A proteolipid protein gene family: Expression in sharks and rays and possible evolution from an ancestral gene encoding a pore-forming polypeptide. Neuron 11:433–448.

    Article  PubMed  CAS  Google Scholar 

  13. Kuhlenberg, H. (1975) The Central Nervous System of Vertebrates Vol. 4: Spinal Cord and Deutoerencephalon. S. Karger, Basel..

    Google Scholar 

  14. Mathisen, P. M., S. Pease, J. Garvey, L. Hood, and C. Readhead. (1993) Identification of an embryonic isoform of myelin basic protein that is expressed widely in the mouse embryo. Proc. Natl. Acad. Sci. USA 90:10125–10129.

    Article  PubMed  CAS  Google Scholar 

  15. Matthieu, J.-M., F. X. Omlin, H. Ginalski-Winkelmann, and B. J. Cooper. (1984) Myelination in the CNS of mid mutant mice: comparison between composition and structure. Dev. Brain Res. 13:149–158.

    Article  CAS  Google Scholar 

  16. Milne, T. J., A. R. Atkins, J. A. Warren, W. P. Auton, and R. Smith. (1990) Shark myelin basic protein: amino acid sequence, secondary structure, and self-association. J. Neurochem 55:950–955.

    Article  PubMed  CAS  Google Scholar 

  17. Nakajima, K., K. Ikenaka, T. Kagawa, J. Aruga, J. Nakao, K. Nakahira, C. Shiota, S. U. Kim, and K. Mikoshiba. (1993) Novel isoforms of mouse myelin basic protein predominantly expressed in embryonic stage. J. Neurochem 60:1554–1563.

    Article  PubMed  CAS  Google Scholar 

  18. Peters, A., S. L. Palay, and H. deF. Webster. (1991) The fine structure of the nervous system: Neurons and their supporting cells. Oxford University Press, New York.

    Google Scholar 

  19. Playford, D. E. and S. A. Dunlop. (1993) A biphasic sequence of myelination in the developing optic nerve of the frog. J. Comp. Neurol. 333:83–93.

    Article  PubMed  CAS  Google Scholar 

  20. Saavedra, R. A., L. Fors, R. H. Aebersold, B. Arden, S. Horvath, J. Sanders, and L. Hood. (1989) The myelin proteins of the shark brain are similar to the myelin proteins of the mammalian peripheral nervous system. J. Mol. Evol. 29:149–156.

    Article  PubMed  CAS  Google Scholar 

  21. Shinowara, N. L., W. B. Beutel, and J. P. Revel. (1980). Comparative analysis of junctions in the myelin sheath of central and peripheral axons of fish, amphibians and mammals: a freeze-fracture study using complementary replicas. J. Neurocytol. 9:15–38.

    Article  PubMed  CAS  Google Scholar 

  22. Spivack, W. D., N. Zhong, S. Salerno, R. A. Saavedra, and R. M. Gould. (1993) Molecular cloning of the myelin basic proteins in the shark, Squalus acanthias, and the ray, Raja erinacia. J. Neurosci. Res. 35:577–584.

    Article  PubMed  CAS  Google Scholar 

  23. Stratmann, A. and G. Jeserich. (1995) Molecular cloning and tissue expression of a cDNA encoding IP1 - a PO-like glycoprotein of trout CNS myelin. J. Neurochem. 64:2427–2436.

    Article  PubMed  CAS  Google Scholar 

  24. Takei, K., K. Kitamura, K. Banno, and K. Uyemura. (1993) Major glycoproteins in carp CNS myelin: Homology to P0 protein with HNK-1/L2 carbohydrate epitope. Neurochem.Int 23:239–248.

    Article  PubMed  CAS  Google Scholar 

  25. Timsit, S., S. Martinez, B. Allinquant, F. Peyron, L. Puelles, and B. Zalc. (1995) Oligodendrocytes originate in a restricted zone of the embryonic ventral neural tube defined by DM-20 mRNA expression. J. Neurosci. 15:1012–1024.

    PubMed  CAS  Google Scholar 

  26. Timsit, S. G., L. Bally-Cuif, D. R. Colrnan, and B. Zalc. (1992) DM-20 mRNA is expressed during the embryonic development of the nervous system of the mouse. J. Neurochem. 58:1172–1175.

    Article  PubMed  CAS  Google Scholar 

  27. Waehneldt, T. V. (1990) Phytogeny of myelin proteins. Ann. NY Acad. Sci. 605:15–28.

    Article  PubMed  CAS  Google Scholar 

  28. Yanes, C., Monzon-Major, M., De Barry, J., Gombos, G. (1992) Myelin and myelinization in the telencephalon and mesencephalon of the lizard, Gallotia galloti as revealed by immunohistochemical localization of myelin basic protein. Anat. Embryol. (Berl.) 185: 475–87.

    Article  CAS  Google Scholar 

  29. Zhang, S.-M., R. Marsh, N. Ratner, and R. Brackenbuiy. (1995) Myelin glycoprotein P0 is expressed at early stages of chicken and rat embryogenesis. J. Neurosci. Res. 40:241–250.

    Article  PubMed  CAS  Google Scholar 

  30. Zopf, D., V. Sonntag, H. Betz, and E. D. Gundelfinger. (1989). Developmental accumulation and heterogeneity of myelin basic protein transcripts in the chick visual system. Glia 2:241–249.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 1997 Springer-Verlag Berlin Heidelberg

About this paper

Cite this paper

Gould, R.M., Spivack, W.D. (1997). CNS Myelination: What can we learn from phylogeny?. In: Jeserich, G., Althaus, H.H., Richter-Landsberg, C., Heumann, R. (eds) Molecular Signaling and Regulation in Glial Cells. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-60669-4_14

Download citation

  • DOI: https://doi.org/10.1007/978-3-642-60669-4_14

  • Publisher Name: Springer, Berlin, Heidelberg

  • Print ISBN: 978-3-642-64501-3

  • Online ISBN: 978-3-642-60669-4

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics