Skip to main content
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1989 May 1;108(5):1909–1915. doi: 10.1083/jcb.108.5.1909

Neural cell adhesion molecule expression is regulated by Schwann cell- neuron interactions in culture

PMCID: PMC2115570  PMID: 2715182

Abstract

To investigate the cellular and molecular signals underlying regulation of cell adhesion molecule expression, the influence of interactions between dorsal root ganglion neurons and Schwann cells on their expression of L1 and N-CAM was quantitated by immunogold electronmicroscopy. The numbers of antibody binding sites on cell surfaces of neurons and glia were compared between pure populations and co-cultures. After 3 d of co-culture, expression of L1 was reduced by 91% on Schwann cells and 36% on neurons, with expression in pure cultures being taken as 100%. N-CAM expression was unchanged on neurons and reduced by 43% on Schwann cells. Within 3 d after removal of neurons from Schwann cell-neuron co-cultures by immunocytolysis, expression of L1 and N-CAM on Schwann cell surfaces increased by 69 and 84%, respectively. Cell surface antigens recognized by an antibody to mouse liver membranes were unchanged in co-cultures. Furthermore, in co- cultures of neurons and sciatic nerve fibroblasts neither of the three antibodies detected any changes in expression of antigens when pure and co-cultures were compared. These observations suggest that adhesion molecules are not only involved in neuron-Schwann cell recognition and neurite outgrowth on Schwann cells (Seilheimer, B., and M. Schachner. 1988. J. Cell Biol. 107: 341-351), but that cell interactions, in turn, modulate the extent of adhesion molecule expression.

Full Text

The Full Text of this article is available as a PDF (2.0 MB).

Selected References

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

  1. BORNSTEIN M. B. Reconstituted rattail collagen used as substrate for tissue cultures on coverslips in Maximow slides and roller tubes. Lab Invest. 1958 Mar-Apr;7(2):134–137. [PubMed] [Google Scholar]
  2. Bixby J. L., Lilien J., Reichardt L. F. Identification of the major proteins that promote neuronal process outgrowth on Schwann cells in vitro. J Cell Biol. 1988 Jul;107(1):353–361. doi: 10.1083/jcb.107.1.353. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bradley W. G., Asbury A. K. Duration of synthesis phase in neuilemma cells in mouse sciatic nerve during degeneration. Exp Neurol. 1970 Feb;26(2):275–282. doi: 10.1016/0014-4886(70)90125-1. [DOI] [PubMed] [Google Scholar]
  4. Buskirk D. R., Thiery J. P., Rutishauser U., Edelman G. M. Antibodies to a neural cell adhesion molecule disrupt histogenesis in cultured chick retinae. Nature. 1980 Jun 12;285(5765):488–489. doi: 10.1038/285488a0. [DOI] [PubMed] [Google Scholar]
  5. Chang S., Rathjen F. G., Raper J. A. Extension of neurites on axons is impaired by antibodies against specific neural cell surface glycoproteins. J Cell Biol. 1987 Feb;104(2):355–362. doi: 10.1083/jcb.104.2.355. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Daniloff J. K., Levi G., Grumet M., Rieger F., Edelman G. M. Altered expression of neuronal cell adhesion molecules induced by nerve injury and repair. J Cell Biol. 1986 Sep;103(3):929–945. doi: 10.1083/jcb.103.3.929. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Davies A. M., Bandtlow C., Heumann R., Korsching S., Rohrer H., Thoenen H. Timing and site of nerve growth factor synthesis in developing skin in relation to innervation and expression of the receptor. 1987 Mar 26-Apr 1Nature. 326(6111):353–358. doi: 10.1038/326353a0. [DOI] [PubMed] [Google Scholar]
  8. Dodd J., Morton S. B., Karagogeos D., Yamamoto M., Jessell T. M. Spatial regulation of axonal glycoprotein expression on subsets of embryonic spinal neurons. Neuron. 1988 Apr;1(2):105–116. doi: 10.1016/0896-6273(88)90194-8. [DOI] [PubMed] [Google Scholar]
  9. EHRMANN R. L., GEY G. O. The growth of cells on a transparent gel of reconstituted rat-tail collagen. J Natl Cancer Inst. 1956 Jun;16(6):1375–1403. [PubMed] [Google Scholar]
  10. Faissner A., Kruse J., Goridis C., Bock E., Schachner M. The neural cell adhesion molecule L1 is distinct from the N-CAM related group of surface antigens BSP-2 and D2. EMBO J. 1984 Apr;3(4):733–737. doi: 10.1002/j.1460-2075.1984.tb01876.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Fraser S. E., Murray B. A., Chuong C. M., Edelman G. M. Alteration of the retinotectal map in Xenopus by antibodies to neural cell adhesion molecules. Proc Natl Acad Sci U S A. 1984 Jul;81(13):4222–4226. doi: 10.1073/pnas.81.13.4222. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Ghandour S., Langley K., Gombos G., Hirn M., Hirsch M. R., Goridis C. A surface marker for murine vascular endothelial cells defined by monoclonal antibody. J Histochem Cytochem. 1982 Feb;30(2):165–170. doi: 10.1177/30.2.7061819. [DOI] [PubMed] [Google Scholar]
  13. Goridis C., Deagostini-Bazin H., Hirn M., Hirsch M. R., Rougon G., Sadoul R., Langley O. K., Gombos G., Finne J. Neural surface antigens during nervous system development. Cold Spring Harb Symp Quant Biol. 1983;48(Pt 2):527–537. doi: 10.1101/sqb.1983.048.01.057. [DOI] [PubMed] [Google Scholar]
  14. Heumann R., Korsching S., Bandtlow C., Thoenen H. Changes of nerve growth factor synthesis in nonneuronal cells in response to sciatic nerve transection. J Cell Biol. 1987 Jun;104(6):1623–1631. doi: 10.1083/jcb.104.6.1623. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Hämmerling G. J., Lemke H., Hämmerling U., Höhmann C., Wallich R., Rajewsky K. Monoclonal antibodies against murine cell surface antigens: anti-H-2, anti-Ia and anti-T cell antibodies. Curr Top Microbiol Immunol. 1978;81:100–106. doi: 10.1007/978-3-642-67448-8_15. [DOI] [PubMed] [Google Scholar]
  16. Jessen K. R., Mirsky R., Morgan L. Myelinated, but not unmyelinated axons, reversibly down-regulate N-CAM in Schwann cells. J Neurocytol. 1987 Oct;16(5):681–688. doi: 10.1007/BF01637659. [DOI] [PubMed] [Google Scholar]
  17. Keilhauer G., Faissner A., Schachner M. Differential inhibition of neurone-neurone, neurone-astrocyte and astrocyte-astrocyte adhesion by L1, L2 and N-CAM antibodies. Nature. 1985 Aug 22;316(6030):728–730. doi: 10.1038/316728a0. [DOI] [PubMed] [Google Scholar]
  18. Korsching S., Thoenen H. Treatment with 6-hydroxydopamine and colchicine decreases nerve growth factor levels in sympathetic ganglia and increases them in the corresponding target tissues. J Neurosci. 1985 Apr;5(4):1058–1061. doi: 10.1523/JNEUROSCI.05-04-01058.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Lagenaur C., Lemmon V. An L1-like molecule, the 8D9 antigen, is a potent substrate for neurite extension. Proc Natl Acad Sci U S A. 1987 Nov;84(21):7753–7757. doi: 10.1073/pnas.84.21.7753. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Lindner J., Rathjen F. G., Schachner M. L1 mono- and polyclonal antibodies modify cell migration in early postnatal mouse cerebellum. 1983 Sep 29-Oct 5Nature. 305(5933):427–430. doi: 10.1038/305427a0. [DOI] [PubMed] [Google Scholar]
  21. Martini R., Schachner M. Immunoelectron microscopic localization of neural cell adhesion molecules (L1, N-CAM, and MAG) and their shared carbohydrate epitope and myelin basic protein in developing sciatic nerve. J Cell Biol. 1986 Dec;103(6 Pt 1):2439–2448. doi: 10.1083/jcb.103.6.2439. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Martini R., Schachner M. Immunoelectron microscopic localization of neural cell adhesion molecules (L1, N-CAM, and myelin-associated glycoprotein) in regenerating adult mouse sciatic nerve. J Cell Biol. 1988 May;106(5):1735–1746. doi: 10.1083/jcb.106.5.1735. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Mirsky R., Jessen K. R., Schachner M., Goridis C. Distribution of the adhesion molecules N-CAM and L1 on peripheral neurons and glia in adult rats. J Neurocytol. 1986 Dec;15(6):799–815. doi: 10.1007/BF01625196. [DOI] [PubMed] [Google Scholar]
  24. 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]
  25. Nieke J., Schachner M. Expression of the neural cell adhesion molecules L1 and N-CAM and their common carbohydrate epitope L2/HNK-1 during development and after transection of the mouse sciatic nerve. Differentiation. 1985;30(2):141–151. doi: 10.1111/j.1432-0436.1985.tb00525.x. [DOI] [PubMed] [Google Scholar]
  26. Noble M., Albrechtsen M., Møller C., Lyles J., Bock E., Goridis C., Watanabe M., Rutishauser U. Glial cells express N-CAM/D2-CAM-like polypeptides in vitro. Nature. 1985 Aug 22;316(6030):725–728. doi: 10.1038/316725a0. [DOI] [PubMed] [Google Scholar]
  27. Persohn E., Schachner M. Immunoelectron microscopic localization of the neural cell adhesion molecules L1 and N-CAM during postnatal development of the mouse cerebellum. J Cell Biol. 1987 Jul;105(1):569–576. doi: 10.1083/jcb.105.1.569. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Pollerberg G. E., Burridge K., Krebs K. E., Goodman S. R., Schachner M. The 180-kD component of the neural cell adhesion molecule N-CAM is involved in cell-cell contacts and cytoskeleton-membrane interactions. Cell Tissue Res. 1987 Oct;250(1):227–236. doi: 10.1007/BF00214676. [DOI] [PubMed] [Google Scholar]
  29. Pollerberg G. E., Schachner M., Davoust J. Differentiation state-dependent surface mobilities of two forms of the neural cell adhesion molecule. Nature. 1986 Dec 4;324(6096):462–465. doi: 10.1038/324462a0. [DOI] [PubMed] [Google Scholar]
  30. Rathjen F. G., Schachner M. Immunocytological and biochemical characterization of a new neuronal cell surface component (L1 antigen) which is involved in cell adhesion. EMBO J. 1984 Jan;3(1):1–10. doi: 10.1002/j.1460-2075.1984.tb01753.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Rohrer H., Sommer I. Simultaneous expression of neuronal and glial properties by chick ciliary ganglion cells during development. J Neurosci. 1983 Aug;3(8):1683–1693. doi: 10.1523/JNEUROSCI.03-08-01683.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Rutishauser U., Watanabe M., Silver J., Troy F. A., Vimr E. R. Specific alteration of NCAM-mediated cell adhesion by an endoneuraminidase. J Cell Biol. 1985 Nov;101(5 Pt 1):1842–1849. doi: 10.1083/jcb.101.5.1842. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Sanes J. R., Schachner M., Covault J. Expression of several adhesive macromolecules (N-CAM, L1, J1, NILE, uvomorulin, laminin, fibronectin, and a heparan sulfate proteoglycan) in embryonic, adult, and denervated adult skeletal muscle. J Cell Biol. 1986 Feb;102(2):420–431. doi: 10.1083/jcb.102.2.420. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Seilheimer B., Schachner M. Regulation of neural cell adhesion molecule expression on cultured mouse Schwann cells by nerve growth factor. EMBO J. 1987 Jun;6(6):1611–1616. doi: 10.1002/j.1460-2075.1987.tb02408.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Seilheimer B., Schachner M. Studies of adhesion molecules mediating interactions between cells of peripheral nervous system indicate a major role for L1 in mediating sensory neuron growth on Schwann cells in culture. J Cell Biol. 1988 Jul;107(1):341–351. doi: 10.1083/jcb.107.1.341. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Sommer I., Schachner M. Monoclonal antibodies (O1 to O4) to oligodendrocyte cell surfaces: an immunocytological study in the central nervous system. Dev Biol. 1981 Apr 30;83(2):311–327. doi: 10.1016/0012-1606(81)90477-2. [DOI] [PubMed] [Google Scholar]
  37. Taniuchi M., Schweitzer J. B., Johnson E. M., Jr Nerve growth factor receptor molecules in rat brain. Proc Natl Acad Sci U S A. 1986 Mar;83(6):1950–1954. doi: 10.1073/pnas.83.6.1950. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Thanos S., Bonhoeffer F., Rutishauser U. Fiber-fiber interaction and tectal cues influence the development of the chicken retinotectal projection. Proc Natl Acad Sci U S A. 1984 Mar;81(6):1906–1910. doi: 10.1073/pnas.81.6.1906. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Tomaselli K. J., Damsky C. H., Reichardt L. F. Interactions of a neuronal cell line (PC12) with laminin, collagen IV, and fibronectin: identification of integrin-related glycoproteins involved in attachment and process outgrowth. J Cell Biol. 1987 Nov;105(5):2347–2358. doi: 10.1083/jcb.105.5.2347. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Yoshino J. E., Mason P. W., DeVries G. H. Developmental changes in myelin-induced proliferation of cultured Schwann cells. J Cell Biol. 1987 Mar;104(3):655–660. doi: 10.1083/jcb.104.3.655. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES