Neuron
Volume 12, Issue 3, March 1994, Pages 509-527
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The schwann cell precursor and its fate: A study of cell death and differentiation during gliogenesis in rat embryonic nerves

https://doi.org/10.1016/0896-6273(94)90209-7Get rights and content

Summary

We have characterized a cell, the Schwann cell precursor, that represents a distinct intermediate differentiation stage in the process by which Schwann cells are generated from neural crest cells. The Schwann cell precursor shows radical differences from Schwann cells which include death regulation, antigenic phenotype, pattern of cell-cell interaction, migratory behavior, and morphology. In the nerves of the rat hind limb, Schwann cells are irreversibly generated from these during a brief period, essentially embryonic days 15–17. We also provide evidence that the survival of Schwann cell precursors is regulated by neurons and identify basic fibroblast growth factor as a potential key regulator of apoptosis in Schwann cell precursors and of precursor to Schwann cell conversion. These findings have implications for our understanding of gliogenesis in the peripheral nervous system.

References (75)

  • HoltonB. et al.

    Analysis of glial cell differentiation in peripheral nervous tissue: I. S100 accumulation in quail embryo spinal ganglion cultures

    Dev. Biol.

    (1982)
  • HoltonB. et al.

    Analysis of glial cell differentiation in peripheral nervous tissue: II. neurons promote S100 synthesis by purified glial precursor cell populations

    Dev. Biol.

    (1982)
  • JessenK.R. et al.

    Schwann cells: early lineage, regulation of proliferation and control of myelin formation

    Curr. Opin. Neurobiol.

    (1992)
  • KalcheimC.

    Basic fibroblast growth factor stimulates survival of nonneuronal cells developing from trunk neural crest

    Dev. Biol.

    (1989)
  • MarusichM.F. et al.

    Development of the neural crest

    Curr. Opin. Genes Dev.

    (1991)
  • MonukiE.S. et al.

    SCIP: a glial POU domain gene regulated by cyclic AMP

    Neuron

    (1989)
  • MosmannT.

    Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays

    J. Immunol. Meth.

    (1983)
  • NicholsD.H. et al.

    Melanogenesis in cultures of peripheral nervous tissue I. The origin and prospective fate of cells giving rise to melanocytes

    Dev. Biol.

    (1977)
  • SasaharaM. et al.

    PDGF B-chain in neurons of the central nervous system, posterior pituitary, and in a trangenic model

    Cell

    (1991)
  • SommerI. et al.

    Monoclonal antibodies (O1 and O4) to oligodendrocyte cell surfaces: an immunocytological study in the central nervous system

    Dev. Biol.

    (1981)
  • StempleD.L. et al.

    Isolation of a stem cell for neurons and glia from the mammalian neural crest

    Cell

    (1992)
  • ThoenenH.

    The changing scene of neurotrophic factors

    Trends Neurosci.

    (1991)
  • WeinbergH.J. et al.

    Studies on the control of myelinogenesis. II. Evidence for neuronal regulation of myelin production

    Brain Res.

    (1976)
  • WyllieA.H. et al.

    Cell death: the significance of apoptosis

    Int. Rev. Cytol.

    (1980)
  • YehH.-J. et al.

    PDGF A-chain gene is expressed by mammalian neurons during development and in maturity

    Cell

    (1991)
  • BannermanP.G. et al.

    Protein growth factor requirements of rat neural crest cells

    J. Neurosci. Res.

    (1993)
  • BartlettP.F. et al.

    Rat neural antigen-2 (Ran-2) a cell surface antigen on astrocytes, ependymal cells, Müller cells and leptomeninges defined by a monoclonal antibody

    Brain Res.

    (1981)
  • BottensteinJ.E. et al.

    Growth of rat neuroblastoma cell line in serum free supplemented medium

    Proc. Natl Acad. Sci. USA

    (1979)
  • BrillG. et al.

    BHK-21 derived cell lines that produce basic fibroblast growth factor, but not parental BHK-21 lines, initiate neuronal differentiation of neural crest progenitors

    Development

    (1992)
  • BungeR.P. et al.

    Linkage between axonal ensheathment and basal lamina production by Schwann cells

    Annu. Rev. Neurosci.

    (1986)
  • ChristieG.A.

    Developmental stages in somite and postsomite embryos, based on external appearance, and including some features of the macroscopic development of the oral cavity

    J. Morphol.

    (1965)
  • CimentG.

    The melanocyte Schwann cell progenitor: a bipotent intermediate in the neural crest lineage

    Comments Dev. Neurobiol.

    (1990)
  • CurtisR. et al.

    Down-regulation of GAP-43 during oligodendrocyte development and lack of expression by astrocytes in vivo: implications for macroglial differentiation

    Eur. J. Neurosci.

    (1991)
  • CurtisR. et al.

    GAP-43 is expressed by nonmyelinforming Schwann cells of the peripheral nervous system

    J. Cell Biol.

    (1992)
  • DavisL.G. et al.
  • De LéonM. et al.

    Differential regulation of S100β and mRNAs coding for S100-like proteins (42A and 42C) during development and after lesion of rat sciatic nerve

    J. Neurosci. Res.

    (1991)
  • DeloulmeJ.C. et al.

    Neuromodulin (GAP43): a neuronal protein kinase C substrate is also present in O-2A glial cell lineage. Characterization of neuromodulin in secondary cultures of oligodendrocytes and comparison with the neuronal antigen

    J. Cell Biol.

    (1990)
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