Hostname: page-component-cd9895bd7-fscjk Total loading time: 0 Render date: 2024-12-25T04:35:12.222Z Has data issue: false hasContentIssue false

Myelin structure and composition of myelinated tissue in the African lungfish

Published online by Cambridge University Press:  08 September 2009

Daniel A. Kirschner*
Affiliation:
Department of Neuropathology, Harvard Medical School, Boston, MA 02115, USA Department of Neuroscience, Children's Hospital, Boston, MA 02115, USA
Jothie Karthigesan
Affiliation:
Department of Neuropathology, Harvard Medical School, Boston, MA 02115, USA Department of Neuroscience, Children's Hospital, Boston, MA 02115, USA
Oscar A. Bizzozero
Affiliation:
Department of Cell Biology and Physiology, University of New Mexico Health Sciences Center, Albuquerque, New Mexico 87131, USA
Bela Kosaras
Affiliation:
Department of Neuropathology, Harvard Medical School, Boston, MA 02115, USA Department of Neuroscience, Children's Hospital, Boston, MA 02115, USA
Hideyo Inouye
Affiliation:
Department of Neuropathology, Harvard Medical School, Boston, MA 02115, USA Department of Neuroscience, Children's Hospital, Boston, MA 02115, USA
*
Correspondence should be addressed to: Professor Daniel A. Kirschner, Biology Department, Boston College, 140 Commonwealth Avenue, Chestnut Hill, MA 02467-3811, USA phone: 617 552 0211 fax: 617 552 2011 email: [email protected]

Abstract

To analyze myelin structure and the composition of myelinated tissue in the African lungfish (Protopterus dolloi), we used a combination of ultrastructural and biochemical techniques. Electron microscopy showed typical multilamellar myelin: CNS sheaths abutted one another, and PNS sheaths were separated by endoneurial collagen. The radial component, prominent in CNS myelin of higher vertebrates, was suggested by the pattern of staining but was poorly organized. The lipid and myelin protein compositions of lungfish tissues more closely resembled those of teleost than those of higher vertebrates (frog, mouse). Of particular note, for example, lungfish glycolipids lacked hydroxy fatty acids. Native myelin periodicities from unfixed nerves were in the range of those for higher vertebrates rather than for teleost fish. Lungfish PNS myelin had wider inter-membrane spaces compared with other vertebrates, and lungfish CNS myelin had spaces that were closer in value to those in mammalian than to amphibian or teleost myelins. The membrane lipid bilayer was narrower in lungfish PNS myelin compared to other vertebrates, whereas in the CNS myelin the bilayer was in the typical range. Lungfish PNS myelin showed typical compaction and swelling responses to incubation in acidic or alkaline hypotonic saline. The CNS myelin, by contrast, did not compact in acidic saline but did swell in the alkaline solution. This lability was more similar to that for the higher vertebrates than for teleost.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2009

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Avila, R.L., Inouye, H., Baek, R., Yin, X., Trapp, B.D., Feltri, M.L. et al. (2005) Structure and stability of internodal myelin in mouse models of hereditary neuropathy. Journal of Neuropathology & Experimental Neurology 64, 976990.CrossRefGoogle ScholarPubMed
Avila, R.L., Tevlin, B.R., Lees, J.P., Inouye, H. and Kirschner, D.A. (2007) Myelin structure and composition in zebrafish. Neurochemical Research 32, 197209.CrossRefGoogle ScholarPubMed
Barbarese, E., Braun, P.E. and Carson, J.H. (1977) Identification of prelarge and presmall basic proteins in mouse myelin and their structural relationship to large and small basic proteins. Proceedings of the National Academy of Sciences of the U.S.A. 74, 33603364.CrossRefGoogle ScholarPubMed
Bemis, W.E., Burggren, W.W., Kemp, N.E. and American Society of Zoologists. (1987) The Biology and Evolution of Lungfishes, New York, NY, A.R. Liss, Inc.Google Scholar
Blaurock, A.E. (1967) Low-Angle X-Ray Diffraction Studies of the Myelin Sheath of Nerve. Ph.D. Dissertation, Department of Biophysics, Ann Arbor, MI, University of Michigan.Google Scholar
Bunow, M.R. and Levin, I.W. (1988) Phase behavior of cerebroside and its fractions with phosphatidylcholines: calorimetric studies. Biochimica et Biophysica Acta 939, 577586.CrossRefGoogle ScholarPubMed
Burggren, W.W. and Johansen, K. (1986) Circulation and respiration in lungfishes (Dipnoi). Journal of Morphology 190, 217236.CrossRefGoogle Scholar
Burgisser, P., Matthieu, J.M., Jeserich, G. and Waehneldt, T.V. (1986) Myelin lipids: a phylogenetic study. Neurochemical Research 11, 12611272.CrossRefGoogle ScholarPubMed
D'Urso, D., Brophy, P.J., Staugaitis, S.M., Gillespie, C.S., Frey, A.B., Stempak, J.G. et al. (1990) Protein zero of peripheral nerve myelin: biosynthesis, membrane insertion, and evidence for homotypic interaction. Neuron 4, 449460.CrossRefGoogle ScholarPubMed
Fewou, S.N., Bussow, H., Schaeren-Wiemers, N., Vanier, M.T., Macklin, W.B., Gieselmann, V. et al. (2005) Reversal of non-hydroxy:alpha-hydroxy galactosylceramide ratio and unstable myelin in transgenic mice overexpressing UDP-galactose:ceramide galactosyltransferase. Journal of Neurochemistry 94, 469481.CrossRefGoogle ScholarPubMed
Ganser, A.L., Kerner, A.L., Brown, B.J., Davisson, M.T. and Kirschner, D.A. (1988) A survey of neurological mutant mice. I. Lipid composition of myelinated tissue in known myelin mutants. Developmental Neuroscience 10, 99122.CrossRefGoogle ScholarPubMed
Greenwood, P.H. (1986) The natural history of African lungfishes. Journal of Morphology 190, 163179.CrossRefGoogle Scholar
Gunther, J. (1976) Impulse conduction in the myelinated giant fibers of the earthworm. Structure and function of the dorsal nodes in the median giant fiber. The Journal of Comparative Neurology 168, 505531.CrossRefGoogle ScholarPubMed
Hartline, D.K. and Colman, D.R. (2007) Rapid conduction and the evolution of giant axons and myelinated fibers. Current Biology 17, R29R35.CrossRefGoogle ScholarPubMed
Heuser, J.E. and Doggenweiler, C.F. (1966) The fine structural organization of nerve fibers, sheaths, and glial cells in the prawn, Palaemonetes vulgaris. Journal of Cell Biology 30, 381403.CrossRefGoogle ScholarPubMed
Inouye, H., Karthigasan, J. and Kirschner, D.A. (1989) Membrane structure in isolated and intact myelins. Biophysical Journal 56, 129137.CrossRefGoogle ScholarPubMed
Inouye, H. and Kirschner, D.A. (1988a) Membrane interactions in nerve myelin. I. Determination of surface charge from effects of pH and ionic strength on period. Biophysical Journal 53, 235245.CrossRefGoogle ScholarPubMed
Inouye, H. and Kirschner, D.A. (1988b) Membrane interactions in nerve myelin: II. Determination of surface charge from biochemical data. Biophysical Journal 53, 247260.CrossRefGoogle ScholarPubMed
Inouye, H. and Kirschner, D.A. (1990) Phylogenetic aspects of myelin structure. In Jeserich, G., Althaus, H.H. and Waehneldt, T.V. (eds) Cellular and Molecular Biology of Myelination, Berlin: Springer-Verlag. NATO ASI Series H43 pp. 372387.Google Scholar
Jeserich, G. and Waehneldt, T.V. (1986a) Bony fish myelin: evidence for common major structural glycoproteins in central and peripheral myelin of trout. Journal of Neurochemistry 46, 525533.CrossRefGoogle ScholarPubMed
Jeserich, G. and Waehneldt, T.V. (1986b) Characterization of antibodies against major fish CNS myelin proteins: immunoblot analysis and immunohistochemical localization of 36K and IP2 proteins in trout nerve tissue. Journal of Neuroscience Research 15, 147158.CrossRefGoogle ScholarPubMed
Joss, J.M. (2006) Lungfish evolution and development. General and Comparative Endocrinology 148, 285289.CrossRefGoogle ScholarPubMed
Karthigasan, J. and Kirschner, D.A. (1988) Membrane interactions are altered in myelin isolated from central and peripheral nervous system tissues. Journal of Neurochemistry 51, 228236.CrossRefGoogle ScholarPubMed
Ki, P.F. and Kishimoto, Y. (1984) The lipid composition of urodele myelin which lacks hydroxycerebroside and hydroxysulfatide. Journal of Neurochemistry 42, 9941000.CrossRefGoogle ScholarPubMed
Ki, P.F., Kishimoto, Y., Lattman, E.E., Stanley, E.F. and Griffin, J.W. (1985) Structure and function of urodele myelin lacking alpha-hydroxy fatty acid-containing galactosphingolipids: slow nerve conduction and unusual myelin thickness. Brain Research 345, 1924.CrossRefGoogle ScholarPubMed
Kirschner, D.A. and Blaurock, A.E. (1992) Organization, phylogenetic variations and dynamic transitions of myelin structure. In Martenson, R.E. (ed.) Myelin: Biology and Chemistry. Boca Raton, CRC Press.Google Scholar
Kirschner, D.A. and Hollingshead, C.J. (1980) Processing for electron microscopy alters membrane structure and packing in myelin. Journal of Ultrastructure Research 73, 211232.CrossRefGoogle ScholarPubMed
Kirschner, D.A., Inouye, H., Ganser, A.L. and Mann, V. (1989) Myelin membrane structure and composition correlated: a phylogenetic study. Journal of Neurochemistry 53, 15991609.CrossRefGoogle ScholarPubMed
Kishimoto, Y. and Hoshi, C. (1972) Isolation, purification, and assay of fatty acids and steroids from nervous system. In Fried, J.R. (ed.) Methods in Neurochemistry, Vol. 3. New York, Marcel Dekker.Google Scholar
Kosaras, B. and Kirschner, D.A. (1990) Radial component of CNS myelin: junctional subunit structure and supramolecular assembly. Journal of Neurocytology 19, 187199.CrossRefGoogle ScholarPubMed
Lee, J., Alrubaian, J. and Dores, R.M. (2006) Are lungfish living fossils? Observation on the evolution of the opioid/orphanin gene family. General and Comparative Endocrinology 148, 306314.CrossRefGoogle ScholarPubMed
Lenz, P.H., Hartline, D.K. and Davis, A.D. (2000) The need for speed. I. Fast reactions and myelinated axons in copepods. Journal of Comparative Physiology [A] 186, 337345.CrossRefGoogle Scholar
Lowry, O.H., Rosebrough, N.J., Farr, A.L. and Randall, R.J. (1951) Protein measurement with the Folin phenol reagent. Journal of Biological Chemistry 193, 265275.CrossRefGoogle ScholarPubMed
Luo, X., Cerullo, J., Dawli, T., Priest, C., Haddadin, Z., Kim, A. et al. (2008) Peripheral myelin of Xenopus laevis: role of electrostatic and hydrophobic interactions in membrane compaction. Journal of Structural Biology 162, 170183.CrossRefGoogle ScholarPubMed
Luo, X., Sharma, D., Inouye, H., Lee, D., Avila, R.L., Salmona, M. et al. (2007) Cytoplasmic domain of human myelin protein zero likely folded as {beta}-structure in compact myelin. Biophysical Journal 92, 15851597.CrossRefGoogle ScholarPubMed
Matthieu, J.M., Eschmann, N., Burgisser, P., Malotka, J. and Waehneldt, T.V. (1986) Expression of myelin proteins characteristic of fish and tetrapods by Polypterus revitalizes long discredited phylogenetic links. Brain Research 379, 137142.CrossRefGoogle ScholarPubMed
Min, Y., Kristiansen, K., Boggs, J.M., Husted, C., Zasadzinski, J.A. and Israelachvili, J. (2009) Interaction forces and adhesion of supported myelin lipid bilayers modulated by myelin basic protein. Proceedings of the National Academy of Sciences of the U.S.A. 106, 31543159.CrossRefGoogle ScholarPubMed
Roots, B.I. and Lane, N.J. (1983) Myelinating glia of earthworm giant axons: thermally induced intramembranous changes. Tissue and Cell 15, 695709.CrossRefGoogle ScholarPubMed
Sarvas, H.O., Milek, D.J., Weise, M.J., Carnow, T.B., Fudenberg, H.H. and Brostoff, S.W. (1980) Radioimmunoassay for the P2 protein of bovine peripheral nerve myelin. Journal of Immunology 124, 557564.CrossRefGoogle ScholarPubMed
Shinowara, N.L., Beutel, W.B. and Revel, J.P. (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. Journal of Neurocytology 9, 1538.CrossRefGoogle ScholarPubMed
Stratmann, A. and Jeserich, G. (1995) Molecular cloning and tissue expression of a cDNA encoding IP1 – a P0-like glycoprotein of trout CNS myelin. Journal of Neurochemistry 64, 24272436.CrossRefGoogle ScholarPubMed
Tamai, Y., Kojima, H., Saito, S., Takayama-Abe, K. and Horichi, H. (1992) Characteristic distribution of glycolipids in gadoid fish nerve tissues and its bearing on phylogeny. Journal of Lipid Research 33, 13511359.CrossRefGoogle ScholarPubMed
Thompson, A.J., Cronin, M.S. and Kirschner, D.A. (2002) Myelin protein zero exists as dimers and tetramers in native membranes of Xenopus laevis peripheral nerve. Journal of Neuroscience Research 67, 766771.CrossRefGoogle ScholarPubMed
Tohyama, Y., Ichimiya, T., Kasama-Yoshida, H., Cao, Y., Hasegawa, M., Kojima, H. et al. (2000) Phylogenetic relation of lungfish indicated by the amino acid sequence of myelin DM20. Brain Research Molecular Brain Research 80, 256259.CrossRefGoogle ScholarPubMed
Tohyama, Y., Kasama-Yoshida, H., Sakuma, M., Kobayashi, Y., Cao, Y., Hasegawa, M. et al. (1999) Gene structure and amino acid sequence of Latimeria chalumnae (coelacanth) myelin DM20: phylogenetic relation of the fish. Neurochemical Research 24, 867873.CrossRefGoogle ScholarPubMed
Trapp, B.D., Mcintyre, L.J., Quarles, R.H., Nonaka, G.I., Moser, A., Moser, H.W. et al. (1980) Biochemical characterization of myelin isolated from the central nervous system of Xenopus tadpoles. Journal of Neurochemistry 34, 12411246.CrossRefGoogle ScholarPubMed
Vance, D.E. and Sweeley, C.C. (1967) Quantitative determination of the neutral glycosyl ceramides in human blood. Journal of Lipid Research 8, 621630.CrossRefGoogle ScholarPubMed
Vinogradov, A.E. (2005) Genome size and chromatin condensation in vertebrates. Chromosoma 113, 362369.CrossRefGoogle ScholarPubMed
Waehneldt, T.V. (1990) Phylogeny of myelin proteins. Annals of the New York Academy of Sciences 605, 1528.CrossRefGoogle ScholarPubMed
Waehneldt, T.V., Matthieu, J.M. and Jeserich, G. (1986a) Appearance of myelin proteins during vertebrate evolution. Neurochemistry International 9, 463474.CrossRefGoogle ScholarPubMed
Waehneldt, T.V., Matthieu, J.M. and Jeserich, G. (1986b) Major central nervous system myelin glycoprotein of the African lungfish (Protopterus dolloi) cross-reacts with myelin proteolipid protein antibodies, indicating a close phylogenetic relationship with amphibians. Journal of Neurochemistry 46, 13871391.CrossRefGoogle ScholarPubMed
Waehneldt, T.V., Matthieu, J.M., Malotka, J. and Joss, J. (1987) A glycosylated proteolipid protein is common to CNS myelin of recent lungfish (Ceratodidae, Lepidosirenidae). Comparative Biochemistry and Physiology B 88, 12091212.CrossRefGoogle ScholarPubMed
Waehneldt, T.V., Stoklas, S., Jeserich, G. and Matthieu, J.M. (1986c) Central nervous system myelin of teleosts: comparative electrophoretic analysis of its proteins by staining and immunoblotting. Comparative Biochemistry and Physiology B 84, 273278.CrossRefGoogle ScholarPubMed
Waxman, S.G. and Bangalore, L. (2004) Electrophysiologic consequences of myelination. In Lazzarini, R.A. (ed.) Myelin Biology and Disorders. Amsterdam: Elsevier/Academic Press, pp. 117141.Google Scholar
Weatherby, T.M., Davis, A.D., Hartline, D.K. and Lenz, P.H. (2000) The need for speed. II. Myelin in calanoid copepods. Journal of Comparative Physiology [A] 186, 347357.CrossRefGoogle ScholarPubMed
Windschiegl, B. and Steinem, C. (2006) Influence of alpha-hydroxylation of glycolipids on domain formation in lipid monolayers. Langmuir 22, 74547457.CrossRefGoogle ScholarPubMed
Xie, B., Luo, X.Y., Zhao, C., Priest, C.M., Chan, S.Y., O'Connor, P.B. et al. (2007) Molecular characterization of myelin protein zero in Xenopus laevis peripheral nerve: equilibrium between non-covalently associated dimer and monomer. International Journal of Mass Spectrometry 268, 304315.CrossRefGoogle ScholarPubMed
Xu, K. and Terakawa, S. (1999) Fenestration nodes and the wide submyelinic space form the basis for the unusually fast impulse conduction of shrimp myelinated axons. The Journal of Experimental Biology 202, 19791989.Google ScholarPubMed
Yoshida, M. and Colman, D.R. (1996) Parallel evolution and coexpression of the proteolipid proteins and protein Zero in vertebrate myelin. Neuron 16, 11151126.CrossRefGoogle ScholarPubMed
Zöller, I., Meixner, M., Hartmann, D., Bussow, H., Meyer, R., Gieselmann, V. et al. (2008) Absence of 2-hydroxylated sphingolipids is compatible with normal neural development but causes late-onset axon and myelin sheath degeneration. Journal of Neuroscience 28, 97419754.CrossRefGoogle ScholarPubMed