Summary
In the PNS, myelin basic protein (MBP) appears not to be essential for myelination, for inshiverer (shi) andmld mutant mice peripheral nerves, where MBP is not or only poorly expressed, myelination occurs normally. Only a few morphological abnormalities, i.e. reduction in axon calibre and myelin sheath thickness, and aberrant Schwann cell-axon contacts, have been reported. Here, we document a consistent difference betweenshi andwild type (wt) myelinated sciatic nerve fibres. The number of Schmidt-Lanterman incisures seen in longitudinally and transversely-sectioned sciatic nerves, or in teased fibres stained for the presence of F-actin, is dramatically increased in homozygousshi mice. With both methods, a twofold increase in Schmidt-Lanterman incisure number is seen in 15-day-old mice, the earliest time examined. The increase is slightly greater in nerve fibres from 30- and 90-day-old mice. The overproduction of Schmidt-Lanterman incisures inshi occurs in spite of the fact that the mean diameter of myelinated fibres inshi sciatic nerves is smaller than inwt sciatic nerves. These results lead us to suggest that the increase in Schmidt-Lanterman incisure density inshi compensates for a defect in Schwann cell-axon communication.
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References
Barbarese, E., Nielson, M. L. &Carson, J. H. (1983) The effect of the shiverer mutation on myelin basic protein expression in homozygous and heterozygous animals.Journal of Neurochemistry 40, 1680–6.
Bennett, V. &Gilligan, D. M. (1993) The spectrin-based membrane skeleton and micron-scale organization of the plasma membrane.Annual Review of Cell Biology 9, 27–66.
Bergoffen, J., Scherer, S. S., Wang, S., Oronzi Scott, M., Bone, L. J., Paul, D. L., Chen, K., Lensch, M. W., Chance, P. F. &Fishbeck, K. H. (1993) Connexin mutations in X-linked Charcot-Marie-Tooth disease.Science 262, 2039–42.
Berthold, C.-H. (1978) Morphology of normal peripheral axons. InPhysiology and Pathobiology of Axons (edited byWaxman, S. G.) pp. 3–63. New York: Raven Press.
Billings-Gagliardi, S. &Wolf, M. K. (1990) Implications of double mutant phenotypes.Annals of the New York Academy of Sciences 605, 215–29.
Blakemore, W. F. (1969) Schmidt-Lanterman incisures in the central nervous system.Journal of Ultrastructure Research 29, 496–8.
Campagnoni, A. T., Pribyl, T. M., Campagnoni, C. W., Kampf, K., Amur-Umarjee, S., Landry, C. F., Handlet, V. W., Newman, S. L., Garbay, B. &Kitamura, K. (1993) Structure and developmental regulation ofGolli-mbp, a 105-kilobase gene that encompasses the myelin basic protein gene and is expressed in cells in the oligodendrocyte lineage in the brain.Journal of Biological Chemistry 268, 4930–8.
Chernoff, G. F. (1981) Shiverer: an autosomal recessive mutant mouse with myelin deficiency.Journal of Heredity 72, 128.
Cramer, L. P., Michison, T. J. &Theriot, J. A. (1994) Actin-dependent motile forces and cell motility.Current Opinion in Cell Biology 6, 92–6.
Einheber, S., Milner, T. A., Giancotti, F. &Salzer, J. L. (1993) Axonal regulation of Schwann cell integrin expression suggests a role for alpha 6 beta 4 in myelination.Journal of Cell Biology 123, 1223–35.
Fath, K. R. &Burgess, D. R. (1994) Membrane motility mediated by unconventional myosin.Current Opinion in Cell Biology 6, 131–5.
Ghabriel, M. N., &Allt, G. (1981) Incisures of Schmidt-Lanterman.Progress in Neurobiology 17, 25–58.
Gould, R. M. &Armstrong, R. (1989) Use of potassium ferrocyanide-reduced osmium tetroxide and lead aspartate in quantitative electron microscopic autoradiography of phospholipids.Journal of Histochemistry and Cytochemistry 37, 1393–9.
Gould, R. M. &Mattingly, G. (1990) Regional localization of RNA, protein and lipid metabolism in Schwann cellsin vivo.Journal of Neurocytology 19, 285–301.
Greenfield, S., Brostoff, S., Eylar, E. H. &Morell, P. (1973) Protein composition of myelin of the peripheral nervous system.Journal of Neurochemistry 20, 1207–16.
Hall, S. M. &Williams, P. L. (1970) Studies on the ‘inciscures’ of Schmidt and Lanterman.Journal of Cell Science 6, 767–91.
Hiscoe, H. B. (1947) Distribution of nodes and incisures in normal and regenerated nerve fibers.Anatomical Record 99, 447–75.
Inoue, Y., Nakamura, R., Mikoshiba, K. &Tsukada, Y. (1981) Fine structure of the central myelin sheath in the myelin deficient mutant shiverer mouse, with special reference to the pattern of myelin formation by oligodendroglia.Brain Research 219, 85–94.
Inouye, H., Ganser, A. L. &Kirschner, D. A. (1985) Shiverer and normal peripheral myelin compared: basic protein localization, membrane interactions, and lipid composition.Journal of Neurochemistry 45, 1911–22.
Kirschner, D. A. &Ganser, A. L. (1980) Compact myelin exists in the absence of basic protein in the shiverer mutant mouse.Nature 299, 357–9.
Kordeli, E., Davis, J., Trapp, B. &Bennett, V. (1990) An isoform of ankyrin is localized at nodes of Ranvier in myelinated axons of central and peripheral nerves.Journal of Cell Biology 11, 1341–52.
Krinke, G., Grieve, A. P. &Schnider, K. (1986) The role of Schmidt-Lanterman incisures in Wallerian degeneration.Acta Neuropathologica 69, 168–70.
Lemke, G. (1988) Unwrapping the genes of myelin.Neuron 1, 535–43.
Mata, M. &Fink, D. (1988) Calmodulin distribution in peripheral nerve: an EM immunocytochemical study.Brain Research 475, 297–304.
Mata, M., Alessi, D. &Fink, D. (1990) S100 is preferentially distributed in myelin-forming Schwann cells.Journal of Neurocytology 19, 432–42.
Mathisen, P. M., Pease, S., Garvey, J., Hood, L. &Readhead, C. (1993) Identification of an embryonic isoform of myelin basic protein that is expressed widely in the mouse embryo.Proceedings of the National Academy of Sciences (USA) 90, 10125–9.
Matthieu, J.-M., Ginalski, H., Friede, R. L., Cohen, S. R. &Doolittle, D. P. (1980a) Absence of myelin basic protein and major dense line in CNS of the mld mutant mouse.Brain Research 191, 278–83.
Matthieu, J.-M., Ginalski, H., Friede, R. L. &Cohen, S. R. (1980b) Low myelin basic protein levels and normal myelin in peripheral nerves of myelin deficient mutant mice (mld).Neuroscience 5, 2315–20.
Matthieu, J. M., Omlin, F. X., Ginalski-Winkelmann, H. &Cooper, B. J. (1984) Myelination in the CNS of mld mutant mice: comparison between composition and structure.Developmental Brain Research 13, 149–58.
Maxwell, W. L., Watt, C., Pediani, J. D., Graham, D. I., Adams, J. H. &Gennarelli, T. A. (1991) Localization of calcium ions and calcium-ATPase activity within myelinated nerve fibres of the adult guinea-pig optic nerve.Journal of Anatomy 176, 71–9.
Mikoshiba, K., Kohsaka, S., Takamatsu, K. &Tsukada, Y. (1981) Neurochemical and morphological studies of the myelin of peripheral nervous system from shiverer mutant mice: absence of basic proteins common to central nervous system.Brain Research 204, 455–60.
Nakajima, K., Ikenaka, K., Kagawa, T., Aruga, J., Nakao, J., Nakahira, K., Shiota, C., Kim, S. U. &Mikoshiba, K. (1993) Novel isoforms of mouse myelin basic protein predominantly expressed in embryonic stage.Glia 60, 1554–63.
Panagopoulos, G., King, R. H. M., Gabriel, G., Stolinski, C., Sofer, D., Lachapelle, F. &Thomas, P. K. (1989) Morphometric and freeze-fracture studies on peripheral nerve in shiverer mice.Journal of Comparative Neurology 286, 337–44.
Peters, A., Palay, S. L. &.Webster, H. De F. (1991)The Fine Structure of the Nervous System: Neurons and their Supporting Cells New York: Oxford University Press.
Peterson, A. C. &Bray, G. M. (1984) Hypomyelination in the peripheral nervous system of shiverer mice and in shiverer-normal chimaera.Journal of Comparative Neurology 227, 348–56.
Pinner, B., Davison, J. F. &Campbell, J. B. (1964) Alkaline phosphatase in peripheral nerve.Science 145, 936–8.
Price, R. L., Lasek, R. J. &Katz, M. J. (1990) Internal áxonal cytoarchitecture is shaped locally by external compressive forces.Brain Research 530, 205–14.
Privat, A., Jacque, C., Bourre, J.-M., Dupouey, P. &Baumann, N. (1979) Absence of the major dense line in myelin of the mutant mouse shiverer.Neuroscience Letters 12, 107–12.
Roach, A., Boylan, K., Horvath, S., Prusiner, S. &Hood, L. (1983) Characterization of cloned cDNA representing rat myelin basic protein: absence of expression in brain of shiverer mutant mice.Cell 34, 799–806.
Robertson, J. D. (1958) The ultrastructure of Schmidt-Lanterman clefts and related shearing defects of the myelin sheath.Journal of Biophysical and Biochemical Cytology 4, 39–46.
Rosenbluth, J. (1980a) Central myelin in the mutant mouse shiverer.Journal of Comparative Neurology 194, 639–48.
Rosenbluth, J. (1980b) Peripheral myelin in the mouse mutant shiverer.Journal of Comparative Neurology 193, 729–39.
Singer, M. (1969) Penetration of labelled amino acids into the peripheral nerve fiber from surrounding body fluids. InGrowth of the Nervous System (edited byWolstenholme, G. E. W. &O'connor, M.) pp. 200–15. London: Churchill.
Singer, M. &Bryant, S. V. (1969) Movement in the myelin Schwann sheath of the vertebrate axon.Nature 221, 1148–50.
Steffensen, S. C., Raymond, S. A., Ganser, A. L. &Strichartz, G. R. (1989) Genetic deletion of myelin basic protein is associated with abnormal latency shifts during repetitive impulse discharge.Society for Neuroscience Abstracts 15, 145.11.
Trapp, B. D., Andrews, S. B., Wong, A., O'Connell, M. &Griffin, J. W. (1989) Co-localization of the myelinassociated glycoprotein and the microfilament components, F-actin and spectrin, in Schwann cells of myelinated nerve fibres.Journal of Neurocytology 18, 47–60.
Webster, H. DE F. (1964) The relationship between Schmidt-Lanterman incisures and myelin segmentation during Wallerian degeneration.Annals of the New York Academy of Sciences 122, 29–38.
Winter, J. (1982) Shiverer peripheral myelin contains P2.Nature 298, 471–2.
Zelenika, D., Grima, B. &Pessac, B. (1993) A new family of transcripts of the myelin basic protein gene: expression in brain and in immune system.Glia 60, 1574–7.
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Gould, R.M., Byrd, A.L. & Barbarese, E. The number of Schmidt-Lanterman incisures is more than doubled inshiverer PNS myelin sheaths. J Neurocytol 24, 85–98 (1995). https://doi.org/10.1007/BF01181552
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DOI: https://doi.org/10.1007/BF01181552