Induction of myelination in the central nervous system by electrical activity (original) (raw)

Abstract

The oligodendrocyte is the myelin-forming cell in the central nervous system. Despite the close interaction between axons and oligodendrocytes, there is little evidence that neurons influence myelinogenesis. On the contrary, newly differentiated oligodendrocytes, which mature in culture in the total absence of neurons, synthesize the myelin-specific constituents of oligodendrocytes differentiated in vivo and even form myelin-like figures. Neuronal electrical activity may be required, however, for the appropriate formation of the myelin sheath. To investigate the role of electrical activity on myelin formation, we have used highly specific neurotoxins, which can either block (tetrodotoxin) or increase (alpha-scorpion toxin) the firing of neurons. We show that myelination can be inhibited by blocking the action potential of neighboring axons or enhanced by increasing their electrical activity, clearly linking neuronal electrical activity to myelinogenesis.

9887

Images in this article

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Aguayo A. J., Charron L., Bray G. M. Potential of Schwann cells from unmyelinated nerves to produce myelin: a quantitative ultrastructural and radiographic study. J Neurocytol. 1976 Oct;5(8):565–573. doi: 10.1007/BF01175570. [DOI] [PubMed] [Google Scholar]
  2. Althaus H. H., Montz H., Neuhoff V., Schwartz P. Isolation and cultivation of mature oligodendroglial cells. Naturwissenschaften. 1984 Jun;71(6):309–315. doi: 10.1007/BF00396614. [DOI] [PubMed] [Google Scholar]
  3. Barres B. A., Chun L. L., Corey D. P. Ion channels in vertebrate glia. Annu Rev Neurosci. 1990;13:441–474. doi: 10.1146/annurev.ne.13.030190.002301. [DOI] [PubMed] [Google Scholar]
  4. Barres B. A., Jacobson M. D., Schmid R., Sendtner M., Raff M. C. Does oligodendrocyte survival depend on axons? Curr Biol. 1993 Aug 1;3(8):489–497. doi: 10.1016/0960-9822(93)90039-q. [DOI] [PubMed] [Google Scholar]
  5. Barres B. A., Raff M. C. Proliferation of oligodendrocyte precursor cells depends on electrical activity in axons. Nature. 1993 Jan 21;361(6409):258–260. doi: 10.1038/361258a0. [DOI] [PubMed] [Google Scholar]
  6. Berwald-Netter Y., Martin-Moutot N., Koulakoff A., Couraud F. Na+-channel-associated scorpion toxin receptor sites as probes for neuronal evolution in vivo and in vitro. Proc Natl Acad Sci U S A. 1981 Feb;78(2):1245–1249. doi: 10.1073/pnas.78.2.1245. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Binder L. I., Frankfurter A., Rebhun L. I. Differential localization of MAP-2 and tau in mammalian neurons in situ. Ann N Y Acad Sci. 1986;466:145–166. doi: 10.1111/j.1749-6632.1986.tb38392.x. [DOI] [PubMed] [Google Scholar]
  8. Bottenstein J. E., Sato G. H. Growth of a rat neuroblastoma cell line in serum-free supplemented medium. Proc Natl Acad Sci U S A. 1979 Jan;76(1):514–517. doi: 10.1073/pnas.76.1.514. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Catterall W. A. Neurotoxins that act on voltage-sensitive sodium channels in excitable membranes. Annu Rev Pharmacol Toxicol. 1980;20:15–43. doi: 10.1146/annurev.pa.20.040180.000311. [DOI] [PubMed] [Google Scholar]
  10. Colello R. J., Devey L. R., Imperato E., Pott U. The chronology of oligodendrocyte differentiation in the rat optic nerve: evidence for a signaling step initiating myelination in the CNS. J Neurosci. 1995 Nov;15(11):7665–7672. doi: 10.1523/JNEUROSCI.15-11-07665.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Dargent B., Couraud F. Down-regulation of voltage-dependent sodium channels initiated by sodium influx in developing neurons. Proc Natl Acad Sci U S A. 1990 Aug;87(15):5907–5911. doi: 10.1073/pnas.87.15.5907. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Dong Z., Brennan A., Liu N., Yarden Y., Lefkowitz G., Mirsky R., Jessen K. R. Neu differentiation factor is a neuron-glia signal and regulates survival, proliferation, and maturation of rat Schwann cell precursors. Neuron. 1995 Sep;15(3):585–596. doi: 10.1016/0896-6273(95)90147-7. [DOI] [PubMed] [Google Scholar]
  13. Dubois-Dalcq M., Behar T., Hudson L., Lazzarini R. A. Emergence of three myelin proteins in oligodendrocytes cultured without neurons. J Cell Biol. 1986 Feb;102(2):384–392. doi: 10.1083/jcb.102.2.384. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. GYLLENSTEN L., MALMFORS T. Myelinization of the optic nerve and its dependence on visual function--a quantitative investigation in mice. J Embryol Exp Morphol. 1963 Mar;11:255–266. [PubMed] [Google Scholar]
  15. Jessen K. R., Mirsky R. Schwann cell precursors and their development. Glia. 1991;4(2):185–194. doi: 10.1002/glia.440040210. [DOI] [PubMed] [Google Scholar]
  16. Kiss J. Z., Wang C., Olive S., Rougon G., Lang J., Baetens D., Harry D., Pralong W. F. Activity-dependent mobilization of the adhesion molecule polysialic NCAM to the cell surface of neurons and endocrine cells. EMBO J. 1994 Nov 15;13(22):5284–5292. doi: 10.1002/j.1460-2075.1994.tb06862.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Linnington C., Webb M., Woodhams P. L. A novel myelin-associated glycoprotein defined by a mouse monoclonal antibody. J Neuroimmunol. 1984 Sep-Oct;6(6):387–396. doi: 10.1016/0165-5728(84)90064-x. [DOI] [PubMed] [Google Scholar]
  18. Lubetzki C., Demerens C., Anglade P., Villarroya H., Frankfurter A., Lee V. M., Zalc B. Even in culture, oligodendrocytes myelinate solely axons. Proc Natl Acad Sci U S A. 1993 Jul 15;90(14):6820–6824. doi: 10.1073/pnas.90.14.6820. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Lubetzki C., Goujet-Zalc C., Demerens C., Danos O., Zalc B. Clonal segregation of oligodendrocytes and astrocytes during in vitro differentiation of glial progenitor cells. Glia. 1992;6(4):289–300. doi: 10.1002/glia.440060407. [DOI] [PubMed] [Google Scholar]
  20. Macklin W. B., Weill C. L., Deininger P. L. Expression of myelin proteolipid and basic protein mRNAs in cultured cells. J Neurosci Res. 1986;16(1):203–217. doi: 10.1002/jnr.490160118. [DOI] [PubMed] [Google Scholar]
  21. Matteoli M., Takei K., Perin M. S., Südhof T. C., De Camilli P. Exo-endocytotic recycling of synaptic vesicles in developing processes of cultured hippocampal neurons. J Cell Biol. 1992 May;117(4):849–861. doi: 10.1083/jcb.117.4.849. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Mirsky R., Winter J., Abney E. R., Pruss R. M., Gavrilovic J., Raff M. C. Myelin-specific proteins and glycolipids in rat Schwann cells and oligodendrocytes in culture. J Cell Biol. 1980 Mar;84(3):483–494. doi: 10.1083/jcb.84.3.483. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Monge M., Kadiiski D., Jacque C. M., Zalc B. Oligodendroglial expression and deposition of four major myelin constituents in the myelin sheath during development. An in vivo study. Dev Neurosci. 1986;8(4):222–235. doi: 10.1159/000112255. [DOI] [PubMed] [Google Scholar]
  24. Notterpek L. M., Rome L. H. Functional evidence for the role of axolemma in CNS myelination. Neuron. 1994 Aug;13(2):473–485. doi: 10.1016/0896-6273(94)90361-1. [DOI] [PubMed] [Google Scholar]
  25. Owens G. C., Bunge R. P. Evidence for an early role for myelin-associated glycoprotein in the process of myelination. Glia. 1989;2(2):119–128. doi: 10.1002/glia.440020208. [DOI] [PubMed] [Google Scholar]
  26. Ozawa K., Suchanek G., Breitschopf H., Brück W., Budka H., Jellinger K., Lassmann H. Patterns of oligodendroglia pathology in multiple sclerosis. Brain. 1994 Dec;117(Pt 6):1311–1322. doi: 10.1093/brain/117.6.1311. [DOI] [PubMed] [Google Scholar]
  27. Pfeiffer S. E., Warrington A. E., Bansal R. The oligodendrocyte and its many cellular processes. Trends Cell Biol. 1993 Jun;3(6):191–197. doi: 10.1016/0962-8924(93)90213-k. [DOI] [PubMed] [Google Scholar]
  28. Prineas J. W., Barnard R. O., Kwon E. E., Sharer L. R., Cho E. S. Multiple sclerosis: remyelination of nascent lesions. Ann Neurol. 1993 Feb;33(2):137–151. doi: 10.1002/ana.410330203. [DOI] [PubMed] [Google Scholar]
  29. Raine C. S., Scheinberg L., Waltz J. M. Multiple sclerosis. Oligodendrocyte survival and proliferation in an active established lesion. Lab Invest. 1981 Dec;45(6):534–546. [PubMed] [Google Scholar]
  30. Reynolds R., Wilkin G. P. Development of macroglial cells in rat cerebellum. II. An in situ immunohistochemical study of oligodendroglial lineage from precursor to mature myelinating cell. Development. 1988 Feb;102(2):409–425. doi: 10.1242/dev.102.2.409. [DOI] [PubMed] [Google Scholar]
  31. Sarlieve L. L., Rao G. S., Campbell G. L., Pieringer R. A. Investigations on myelination in vitro: biochemical and morphological changes in cultures of dissociated brain cells from embryonic mice. Brain Res. 1980 May 5;189(1):79–90. doi: 10.1016/0006-8993(80)90008-6. [DOI] [PubMed] [Google Scholar]
  32. Scherer Martin, Heller Martin, Schachner Melitta. Expression of the Neural Recognition Molecule L1 by Cultured Neural Cells is influenced by K+ and the Glutamate Receptor Agonist NMDA. Eur J Neurosci. 1992;4(6):554–562. doi: 10.1111/j.1460-9568.1992.tb00905.x. [DOI] [PubMed] [Google Scholar]
  33. Scherer S. S., Vogelbacker H. H., Kamholz J. Axons modulate the expression of proteolipid protein in the CNS. J Neurosci Res. 1992 Jun;32(2):138–148. doi: 10.1002/jnr.490320203. [DOI] [PubMed] [Google Scholar]
  34. Scherer S. S., Wang D. Y., Kuhn R., Lemke G., Wrabetz L., Kamholz J. Axons regulate Schwann cell expression of the POU transcription factor SCIP. J Neurosci. 1994 Apr;14(4):1930–1942. doi: 10.1523/JNEUROSCI.14-04-01930.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Shatz C. J. Impulse activity and the patterning of connections during CNS development. Neuron. 1990 Dec;5(6):745–756. doi: 10.1016/0896-6273(90)90333-b. [DOI] [PubMed] [Google Scholar]
  36. Szuchet S., Polak P. E., Yim S. H. Mature oligodendrocytes cultured in the absence of neurons recapitulate the ontogenic development of myelin membranes. Dev Neurosci. 1986;8(4):208–221. doi: 10.1159/000112254. [DOI] [PubMed] [Google Scholar]
  37. Tauber H., Waehneldt T. V., Neuhoff V. Myelination in rabbit optic nerves is accelerated by artificial eye opening. Neurosci Lett. 1980 Mar;16(3):235–238. doi: 10.1016/0304-3940(80)90003-8. [DOI] [PubMed] [Google Scholar]
  38. Wiesel T. N., Hubel D. H. Comparison of the effects of unilateral and bilateral eye closure on cortical unit responses in kittens. J Neurophysiol. 1965 Nov;28(6):1029–1040. doi: 10.1152/jn.1965.28.6.1029. [DOI] [PubMed] [Google Scholar]
  39. Wood P. M., Bunge R. P. Evidence that axons are mitogenic for oligodendrocytes isolated from adult animals. Nature. 1986 Apr 24;320(6064):756–758. doi: 10.1038/320756a0. [DOI] [PubMed] [Google Scholar]
  40. Wood P. M., Williams A. K. Oligodendrocyte proliferation and CNS myelination in cultures containing dissociated embryonic neuroglia and dorsal root ganglion neurons. Brain Res. 1984 Feb;314(2):225–241. doi: 10.1016/0165-3806(84)90045-2. [DOI] [PubMed] [Google Scholar]