Skip to main content
PMC home page
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1980 Mar 1;84(3):753–766. doi: 10.1083/jcb.84.3.753

Studies of Schwann cell proliferation. II. Characterization of the stimulation and specificity of the response to a neurite membrane fraction

PMCID: PMC2110566  PMID: 7358797

Abstract

When prepared by methods utilized in our laboratory, pure populations of Schwann cells in culture do not divide, but, after recombination with peripheral sensory neurons or their processes, proliferate rapidly (Wood and Bunge, 1975, Nature (Lond.) 256:661--664). In this paper, we demonstrate that a membrane fraction prepared from sensory ganglion neurites is also mitogenic for Schwann cells and increases the labeling index (assessed by autoradiography after incubation of cells with tritiated thymidine) from less than 0.2 to 10% for primary cells, and from 0.4 to 18--19% for replated cells. The increased responsiveness of replated cells may reflect their greater access to the neurite membranes which is a consequence of the elimination of multiple cell layers after replating and the removal of the basal lamina. This stimulation was specific; addition of membrane preparations from other cell types (3T3, C1300, etc.) was not mitogenic. Ultrastructural analysis demonstrated apparent binding of neurite membranes to Schwann cells as well as significant phagocytosis of the membranes by the cells. The uptake of nonmitogenic membranes suggests that phagocytosis per se is not the stimulus of proliferation.

Full Text

The Full Text of this article is available as a PDF (1.5 MB).

Selected References

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

  1. Barnes D. W., Colowick S. P. Stimulation of sugar uptake and thymidine incorporation in mouse 3T3 cells by calcium phosphate and other extracellular particles. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5593–5597. doi: 10.1073/pnas.74.12.5593. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Berner A., Torvik A., Stenwig A. E. Origin of macrophages in traumatic lesions and Wallerian degeneration in peripheral nerves. Acta Neuropathol. 1973;25(3):228–236. doi: 10.1007/BF00685202. [DOI] [PubMed] [Google Scholar]
  3. Bunge M. B. Initial endocytosis of perioxidase or ferritin by growth cones of cultured nerve cells. J Neurocytol. 1977 Aug;6(4):407–439. doi: 10.1007/BF01178226. [DOI] [PubMed] [Google Scholar]
  4. Bunge M. B., Williams A. K., Wood P. M., Uitto J., Jeffrey J. J. Comparison of nerve cell and nerve cell plus Schwann cell cultures, with particular emphasis on basal lamina and collagen formation. J Cell Biol. 1980 Jan;84(1):184–202. doi: 10.1083/jcb.84.1.184. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bunge R. P., Bunge M. B. Evidence that contact with connective tissue matrix is required for normal interaction between Schwann cells and nerve fibers. J Cell Biol. 1978 Sep;78(3):943–950. doi: 10.1083/jcb.78.3.943. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bunge R. P., Wood P. Studies on the transplantation of spinal cord tissue in the rat. I. The development of a culture system for hemisections of embryonic spinal cord. Brain Res. 1973 Jul 27;57(2):261–276. doi: 10.1016/0006-8993(73)90135-2. [DOI] [PubMed] [Google Scholar]
  7. DJORDJEVIC B., SZYBALSKI W. Genetics of human cell lines. III. Incorporation of 5-bromo- and 5-iododeoxyuridine into the deoxyribonucleic acid of human cells and its effect on radiation sensitivity. J Exp Med. 1960 Sep 1;112:509–531. doi: 10.1084/jem.112.3.509. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. FISHER E. R., TURANO A. Schwann cells in wallerian degeneration. Arch Pathol. 1963 May;75:517–527. [PubMed] [Google Scholar]
  9. Holtzman E., Novikoff A. B. Lysomes in the rat sciatic nerve following crush. J Cell Biol. 1965 Dec;27(3):651–669. doi: 10.1083/jcb.27.3.651. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Lawson S. N., Caddy K. W., Biscoe T. J. Development of rat dorsal root ganglion neurones. Studies of cell birthdays and changes in mean cell diameter. Cell Tissue Res. 1974;153(3):399–413. doi: 10.1007/BF00229167. [DOI] [PubMed] [Google Scholar]
  11. Masurovsky E. B., Bunge M. B., Bunge R. P. Cytological studies of organotypic cultures of rat dorsal root ganglia following X-irradiation in vitro. I. Changes in neurons and satellite cells. J Cell Biol. 1967 Feb;32(2):467–496. doi: 10.1083/jcb.32.2.467. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. NATHANIEL E. J. PEASE DC: DEGENERATIVE CHANGES IN RAT DORSAL ROOTS DURING WALLERIAN DEGENERATION. J Ultrastruct Res. 1963 Dec;52:511–532. doi: 10.1016/s0022-5320(63)80082-9. [DOI] [PubMed] [Google Scholar]
  13. Romine J. S., Bray G. M., Aguayo A. J. Schwann cell multiplication after crush injury of unmyelinated fibers. Arch Neurol. 1976 Jan;33(1):49–54. doi: 10.1001/archneur.1976.00500010051008. [DOI] [PubMed] [Google Scholar]
  14. Rubin H., Sanui H. Complexes of inorganic pyrophosphate, orthophosphate, and calcium as stimulants of 3T3 cell multiplication. Proc Natl Acad Sci U S A. 1977 Nov;74(11):5026–5030. doi: 10.1073/pnas.74.11.5026. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. SATINSKY D., PEPE F. A., LIU C. N. THE NEURILEMMA CELL IN PERIPHERAL NERVE DEGENERATION AND REGENERATION. Exp Neurol. 1964 Jun;9:441–451. doi: 10.1016/0014-4886(64)90052-4. [DOI] [PubMed] [Google Scholar]
  16. Salzer J. L., Bunge R. P., Glaser L. Studies of Schwann cell proliferation. III. Evidence for the surface localization of the neurite mitogen. J Cell Biol. 1980 Mar;84(3):767–778. doi: 10.1083/jcb.84.3.767. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Salzer J. L., Bunge R. P. Studies of Schwann cell proliferation. I. An analysis in tissue culture of proliferation during development, Wallerian degeneration, and direct injury. J Cell Biol. 1980 Mar;84(3):739–752. doi: 10.1083/jcb.84.3.739. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Schubert D., Heinemann S., Carlisle W., Tarikas H., Kimes B., Patrick J., Steinbach J. H., Culp W., Brandt B. L. Clonal cell lines from the rat central nervous system. Nature. 1974 May 17;249(454):224–227. doi: 10.1038/249224a0. [DOI] [PubMed] [Google Scholar]
  19. Schubert D., Humphreys S., Jacob F., de Vitry F. Induced differentiation of a neuroblastoma. Dev Biol. 1971 Aug;25(4):514–546. doi: 10.1016/0012-1606(71)90004-2. [DOI] [PubMed] [Google Scholar]
  20. Terry L. C., Bray G. M., Aguayo A. J. Schwann cell multiplication in developing rat unmyelinated nerves-a radioautographic study. Brain Res. 1974 Mar 29;69(1):144–148. doi: 10.1016/0006-8993(74)90380-1. [DOI] [PubMed] [Google Scholar]
  21. Varon S. S., Bunge R. P. Trophic mechanisms in the peripheral nervous system. Annu Rev Neurosci. 1978;1:327–361. doi: 10.1146/annurev.ne.01.030178.001551. [DOI] [PubMed] [Google Scholar]
  22. Wood P. M. Separation of functional Schwann cells and neurons from normal peripheral nerve tissue. Brain Res. 1976 Oct 22;115(3):361–375. doi: 10.1016/0006-8993(76)90355-3. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Cell Biology are provided here courtesy of The Rockefeller University Press

RESOURCES