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.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Preview
Unable to display preview. Download preview PDF.
References
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.
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.
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.
Chapman, E. R. and R. Jahn. (1994) Calcium-dependent interaction of the cytoplasmic region of synaptotagmin with membranes. J. Biol. Chem. 269:5735–5741.
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.
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.
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.
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.
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.
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.
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.
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.
Kuhlenberg, H. (1975) The Central Nervous System of Vertebrates Vol. 4: Spinal Cord and Deutoerencephalon. S. Karger, Basel..
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Waehneldt, T. V. (1990) Phytogeny of myelin proteins. Ann. NY Acad. Sci. 605:15–28.
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.
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.
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.
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Rights 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