Journal of Neurocytology

, Volume 21, Issue 9, pp 635–647 | Cite as

Division and migration of satellite glia in the embryonic rat superior cervical ganglion

  • A. K. Hall
  • S. C. Landis


While distinct precursors committed to a neuronal or glial cell fate are generated from neural crest cells early in peripheral gangliogenesis, little is known about the subsequent generation and maturation of young satellite glia from restricted glial precursor cells. To examine the division and migration of glial precursor cells and their satellite cell progeny, morphological, immunocytochemical and culture techniques were applied to the developing rat superior cervical ganglion. At embryonic day (E)18.5, numerous clusters of nonneuronal cells appeared transiently in the ganglion. Individual cells with a similar morphology were present in E16.5 ganglia, and are likely to represent the precursor cells which generate these clusters. The clustered cells were distinguishable from neighbouring neurons as well as from endothelial cells and fibroblasts. Morphologically similar cells were present in nerve bundles at E18.5 and surrounding principal neurons and nerve bundles in the adult ganglion. Double-label studies of the E18.5 ganglion with tyrosine hydroxylase to identify noradrenergic neurons and propidium iodide counterstaining to visualize all cell nuclei revealed that the cells in clusters stained with propidium iodide but lacked tyrosine hydroxylase immunoreactivity. To determine if cell clusters arose from division, bromodeoxyuridine, a thymidine analogue, was administered to pregnant mothers between E16.5–E18.5, and ganglionic cells examined at E18.5 bothin vivo andin vitro. Numerous non-neuronal cells divided during this periodin situ and composed portions of clusters. When dissociated, superior cervical ganglion satellite glia reacted with an NGF-receptor antibody (MAb 217c) and possessed a flattened shape, in contrast to bipolar Schwann cells. Over half of the 217c-immunoreactive glia at E18.5 had incorporated bromodeoxyuridine during E16.5–18.5in vivo. At birth, non-neuronal cells were no longer grouped in clusters, but were associated with neuronal cell bodies and processes. These findings suggest that, between E16.5–E18.5, glial precursors divide rapidly to form clusters, and that, after the peak of neurogenesis, daughter cells migrate within the ganglion to associate with nerve cell bodies and processes where proliferation continues at a slower rate. Distinct cellular and molecular interactions are likely to trigger the initial rapid division of glial precursors, initiate their migration and association with neuron cell bodies, and control their subsequent slower division.


Tyrosine Hydroxylase Neural Crest Cell Bromodeoxyuridine Superior Cervical Ganglion Nerve Bundle 
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  1. Aguayo, A. J., Peyronnard, J. M., Terry, L. C., Romine, J. C. &Bray, G. M. (1976a) Neonatal neuronal loss in rat superior cervical ganglia; retrograde effects on developing preganglionic axons and Schwann cells.Journal of Neurocytology 5, 137–55.Google Scholar
  2. Aguayo, A. J., Charron, L. &Bray, G. M. (1976b) Potential of Schwann cells from unmyelinated nerves to produce myelin: a quantitative ultrastructural and radiographic study.Journal of Neurocytology 5, 565–73.Google Scholar
  3. Anderson, D. J. &Axel, R. (1985) Molecular probes for the development and plasticity of neural crest derivatives.Cell 42, 649–62.Google Scholar
  4. Bronner-Fraser, M. &Fraser, S. (1988) Cell lineage analysis reveals multipotency of some avian neural crest cells.Nature 335, 161–4.Google Scholar
  5. Bunge, R. P., Bunge, M. B. &Eldridge, C. F. (1986) Linkage between axonal ensheathment and basal lamina production by Schwann cells.Annual Review of Neuroscience 9, 305–28.Google Scholar
  6. Christie, G. A. (1962) Developmental stages in somite and post somite rat embryos based on external appearance, and including some features of the macroscopic development of the oral cavity.Journal of Morphology 114, 263–86.Google Scholar
  7. Decoster, M. A. &Devries, G. H. (1989) Evidence that the axolemmal mitogen for cultured Schwann cells is a positively charged, heparan sulfate proteoglycan-bound, heparin-displaceable molecule.Journal of Neuroscience Research 22, 283–8.Google Scholar
  8. Distefano, P. S. &Johnson, E. M. (1988) Nerve growth factor receptors on cultured rat Schwann cells.Journal of Neuroscience 8, 231–41.Google Scholar
  9. Dulac, C., Cameron-Curry, P., Ziller, C. &Ledouarin, N. M. (1988) A surface protein expressed by avian myelinating and nonmyelinating Schwann cells but not by satellite or enteric glial cells.Neuron 1, 211–20.Google Scholar
  10. Faissner, A., Kruse, J., Nieke, J. &Schachner, M. (1984) Expression of neural cell adhesion molecular L1 during development, in neurological mutants and in the peripheral nervous system.Developmental Brain Research 15, 69–82.Google Scholar
  11. Frank, E. &Sanes, J. R. (1991) Lineage of neurons and glia in chick dorsal root ganglia: analysisin vivo with a recombinant retrovirus.Development 111, 895–908.Google Scholar
  12. Giloh, H. &Sedat, J. W. (1982) Fluorescence microscopy: reduced photobleaching of rhodamine and fluorescein protein conjugates by n-propyl gallate.Science 217, 1252–5.Google Scholar
  13. Gratzner, H. G. (1982) A new reagent for detection of DNA replication.Science 218, 474–5.Google Scholar
  14. Hall, A. K. &Landis, S. C. (1991) Early commitment of precursor cells from the rat superior cervical ganglion to neuronal or nonneuronal fates.Neuron 6, 741–52.Google Scholar
  15. Hawrot, E. &Patterson, P. H. (1979) Long-term culture of dissociated sympathetic neurons.Methods in Enzymology 53, 574–84.Google Scholar
  16. Hendry, I. (1977) Cell division in the developing sympathetic nervous system.Journal of Neurocytology 6, 299–309.Google Scholar
  17. Hendry, I. &Campbell, J. (1976) Morphometric analysis of the rat superior cervical ganglion after axotomy and nerve growth factor treatment.Journal of Neurocytology 5, 351–60.Google Scholar
  18. Houck, D. W. &Loken, M. R. (1985) The simultaneous analysis of cell surface antigens, bromodeoxyuridine and DNA content.Cytometry,6, 531–8.Google Scholar
  19. Jessen, K. R., Morgan, L., Stewart, H. I. S. &Mirsky, R. (1990) Three markers of adult non-myelin-forming Schwann cells, 217c (Ran-1), ASE3 and GFAP: development and regulation by neuron-Schwann cell interactions.Development 109, 91–103.Google Scholar
  20. Kumar, S., Huber, J., Pena, L. A., Perez-Polo, J. R., Werrbach-Perez, K. &De Vellis, J. (1990) Characterization of functional nerve growth factor receptor in a central nervous system glial cell line: monoclonal antibody 217c recognizes the nerve growth factor receptor on C6 glioma cells.Journal of Neuroscience Research 27, 408–17.Google Scholar
  21. Landis, S. C. &Damboise, S. (1986) Neuron birthdays in the paravertebral sympathetic chain of the rat.Anatomical Record 214, A71.Google Scholar
  22. Lawson, S. N., Caddy, K. W. T. &Biscoe, T. J. (1974) Development of rat dorsal root ganglion neurons: studies of cell birthdays and changes in mean cell diameter.Cell and Tissue Research 153, 399–413.Google Scholar
  23. Le Douarin, N. M. (1982)The Neural Crest Cambridge: Cambridge University Press.Google Scholar
  24. Mccarthy, K. D. &Partlow, L. M. (1976) Neuronal stimulation of (3H) thymidine incorporation by primary cultures of highly purified non-neuronal cells.Brain Research 114, 415–26.Google Scholar
  25. Mirsky, R., Jessen, K. R., Schachner, M. &Goridis, C. (1986) Distribution of the adhesion molecules N-CAM and L1 on peripheral neurons and glia in adult rats.Journal of Neurocytology 15, 799–815.Google Scholar
  26. Nowakowski, R. S., Lewin, S. B. &Miller, M. W. (1989) Bromodeoxyuridine immunohistochemical determination of the lengths of the cell cycle and the DNA-synthetic phase for an anatomically defined population.Journal of Neurocytology 18, 311–18.Google Scholar
  27. Packard, D. S., Menzies, R. A. &Skalko, R. G. (1973) Incorporation of thymidine and its analogue, bromodeoxyuridine, into embryos and maternal tissues of the mouse.Differentiation 1, 397–405.Google Scholar
  28. Pannese, E. (1981) The satellite cells of the sensory ganglia.Advances in Anatomy, Embryology and Cell Biology 65, 1–111.Google Scholar
  29. Peng, W. W., Bressler, J. P., Tiffany-Castiglioni, E. &De Vellis, J. (1982) Development of a monoclonal antibody against a tumour associated antigen.Science 215, 1102–4.Google Scholar
  30. Peters, A. &Muir, A. R. (1959) The relationship between axons and Schwann cells during development of peripheral nerves in the rat.Quarterly Journal of Experimental Physiology 44, 117–30.Google Scholar
  31. Pomeroy, S. L. &Purves, D. (1988) Neuron/glia relationships observed over intervals of several months in living mice.Journal of Cell Biology 107, 1167–75.Google Scholar
  32. Raff, M. C., Abney, E., Brockes, J. P. &Hornby-Smith, A. (1978) Schwann cell growth factors.Cell 15, 813–22.Google Scholar
  33. Ratner, N., Bunge, R. P. &Glaser, L. (1985) A neuronal cell surface heparan sulfate proteoglycan is required for dorsal root ganglion neuron stimulation of Schwann cell proliferation.Journal of Cell Biology 101, 744–54.Google Scholar
  34. Roufa, D., Bunge, M. B., Johnson, M. I. &Cornbrooks, C. J. (1986) Variation in content and function of nonneuronal cells in the outgrowth of sympathetic ganglia from embryos of differing age.Journal of Neuroscience 6, 790–802.Google Scholar
  35. Rubin, E. (1985a) Development of the rat superior cervical ganglion: ganglion cell maturation.Journal of Neuroscience 5, 673–84.Google Scholar
  36. Rubin, E. (1985b) Development of the rat superior cervical ganglion: initial stages of synapse formation.Journal of Neuroscience 5, 697–704.Google Scholar
  37. Salzer, J. L., Bunge, R. P. &Glaser, L. (1980) Studies of Schwann cell proliferation. III. Evidence for the surface localization of the neurite mitogen.Journal of Cell Biology 84, 767–78.Google Scholar
  38. Stemple, D. L. &Anderson, D. J. (1989) Lineage diversification of the neural crest (abstract).Journal of Cell Biology 109, 59a.Google Scholar
  39. Thibault, J., Vidal, D. &Gros, F. (1981)In vitro translation of mRNA from rat pheochromochytoma tumors, characterization of tyrosine hydroxylase.Biochemical and Biophysical Research Communication 99, 960–8.Google Scholar
  40. Vogel, K. S. &Weston, J. A. (1988) A subpopulation of cultured avian neural crest cells has transient neurogenic potential.Neuron 1, 569–77.Google Scholar
  41. Webster, H. Def. (1975) Development of peripheral myelinated and unmyelinated nerve fibres. InPeripheral Neuropathy (edited byDyck, P. J., Thomas, P. K. &Lambert, E. H.). Philadelphia: Saunders.Google Scholar
  42. Weston, J. A. (1963) A radioautographic analysis of the migration and localization of trunk neural crest cells in the chick.Developmental Biology 6, 279–310.Google Scholar
  43. Wood, P. M. &Bunge, R. P. (1975) Evidence that sensory axons are mitogenic for Schwann cells.Nature 256, 662–4.Google Scholar
  44. Yasuda, T., Sobue, G., Mokuno, K., Kreider, B. &Pleasure, D. (1987) Cultured rat Schwann cells express low affinity receptors for nerve growth factor.Brain Research 436, 113–19.Google Scholar
  45. Zimmerman, A. &Sutter, A. (1983) b-nerve growth factor (bNGF) receptors on glial cells. Cell-cell interaction between neurones and Schwann cells in cultures of chick sensory ganglia.EMBO Journal 2, 879–85.Google Scholar

Copyright information

© Chapman and Hall Ltd 1992

Authors and Affiliations

  • A. K. Hall
    • 1
  • S. C. Landis
    • 1
  1. 1.Department of NeurosciencesCase Western Reserve University School of MedicineClevelandUSA

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