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Selective expression of the 180-kD component of the neural cell adhesion molecule N-CAM during development

Abstract

The rodent neural cell adhesion molecule (N-CAM) consists of three glycoprotein chains of 180, 140, and 120 kD in their adult forms. Although the proportions of the three components are known to change during development and differ between brain regions, their individual distribution and function are unknown. Here we report studies carried out with a monoclonal antibody that specifically recognizes the 180-kD component of mouse N-CAM (N-CAM180) in its highly sialylated embryonic and less glycosylated adult forms. In primary cerebellar cell cultures, N-CAM180 antibody reacts intracellularly with all types of neural cells including astrocytes, oligodendrocytes, and neurons. During cerebellar, telencephalic, and retinal development N-CAM180 is detectable by indirect immunohistology in differentiated neural cells, but, in contrast to total N-CAM, not in their proliferating precursors in the ventricular zone and primordial and early postnatal external granular layer. In monolayer cultures of C1300 neuroblastoma cells, N-CAM180 appears by immunofluorescence more concentrated at contact points between adjacent cells, while N-CAM comprising the 180- and 140-kD component shows a more uniform distribution at the plasma membrane. Treatment of neuroblastoma cells with dimethylsulfoxide, which promotes differentiation, induces a shift toward the predominant expression of N- CAM180. These observations support the notion that N-CAM180 is expressed selectively in more differentiated neural cells and suggest a differential role of N-CAM180 in the stabilization of cell contacts.

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Selected References

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  1. Amano T., Richelson E., Nirenberg M. Neurotransmitter synthesis by neuroblastoma clones (neuroblast differentiation-cell culture-choline acetyltransferase-acetylcholinesterase-tyrosine hydroxylase-axons-dendrites). Proc Natl Acad Sci U S A. 1972 Jan;69(1):258–263. doi: 10.1073/pnas.69.1.258. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Burnette W. N. "Western blotting": electrophoretic transfer of proteins from sodium dodecyl sulfate--polyacrylamide gels to unmodified nitrocellulose and radiographic detection with antibody and radioiodinated protein A. Anal Biochem. 1981 Apr;112(2):195–203. doi: 10.1016/0003-2697(81)90281-5. [DOI] [PubMed] [Google Scholar]
  3. 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]
  4. Chuong C. M., Edelman G. M. Alterations in neural cell adhesion molecules during development of different regions of the nervous system. J Neurosci. 1984 Sep;4(9):2354–2368. doi: 10.1523/JNEUROSCI.04-09-02354.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Chuong C. M., McClain D. A., Streit P., Edelman G. M. Neural cell adhesion molecules in rodent brains isolated by monoclonal antibodies with cross-species reactivity. Proc Natl Acad Sci U S A. 1982 Jul;79(13):4234–4238. doi: 10.1073/pnas.79.13.4234. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Cunningham B. A., Hoffman S., Rutishauser U., Hemperly J. J., Edelman G. M. Molecular topography of the neural cell adhesion molecule N-CAM: surface orientation and location of sialic acid-rich and binding regions. Proc Natl Acad Sci U S A. 1983 May;80(10):3116–3120. doi: 10.1073/pnas.80.10.3116. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Edelman G. M., Chuong C. M. Embryonic to adult conversion of neural cell adhesion molecules in normal and staggerer mice. Proc Natl Acad Sci U S A. 1982 Nov;79(22):7036–7040. doi: 10.1073/pnas.79.22.7036. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Edelman G. M. Modulation of cell adhesion during induction, histogenesis, and perinatal development of the nervous system. Annu Rev Neurosci. 1984;7:339–377. doi: 10.1146/annurev.ne.07.030184.002011. [DOI] [PubMed] [Google Scholar]
  9. Eng L. F., Vanderhaeghen J. J., Bignami A., Gerstl B. An acidic protein isolated from fibrous astrocytes. Brain Res. 1971 May 7;28(2):351–354. doi: 10.1016/0006-8993(71)90668-8. [DOI] [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. Finne J., Finne U., Deagostini-Bazin H., Goridis C. Occurrence of alpha 2-8 linked polysialosyl units in a neural cell adhesion molecule. Biochem Biophys Res Commun. 1983 Apr 29;112(2):482–487. doi: 10.1016/0006-291x(83)91490-0. [DOI] [PubMed] [Google Scholar]
  12. Gennarini G., Hirn M., Deagostini-Bazin H., Goridis C. Studies on the transmembrane disposition of the neural cell adhesion molecule N-CAM. The use of liposome-inserted radioiodinated N-CAM to study its transbilayer orientation. Eur J Biochem. 1984 Jul 2;142(1):65–73. doi: 10.1111/j.1432-1033.1984.tb08251.x. [DOI] [PubMed] [Google Scholar]
  13. Grumet M., Rutishauser U., Edelman G. M. Neural cell adhesion molecule is on embryonic muscle cells and mediates adhesion to nerve cells in vitro. Nature. 1982 Feb 25;295(5851):693–695. doi: 10.1038/295693a0. [DOI] [PubMed] [Google Scholar]
  14. Hawkes R., Niday E., Gordon J. A dot-immunobinding assay for monoclonal and other antibodies. Anal Biochem. 1982 Jan 1;119(1):142–147. doi: 10.1016/0003-2697(82)90677-7. [DOI] [PubMed] [Google Scholar]
  15. Hoffman S., Edelman G. M. Kinetics of homophilic binding by embryonic and adult forms of the neural cell adhesion molecule. Proc Natl Acad Sci U S A. 1983 Sep;80(18):5762–5766. doi: 10.1073/pnas.80.18.5762. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hoffman S., Sorkin B. C., White P. C., Brackenbury R., Mailhammer R., Rutishauser U., Cunningham B. A., Edelman G. M. Chemical characterization of a neural cell adhesion molecule purified from embryonic brain membranes. J Biol Chem. 1982 Jul 10;257(13):7720–7729. [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. Kimhi Y., Palfrey C., Spector I., Barak Y., Littauer U. Z. Maturation of neuroblastoma cells in the presence of dimethylsulfoxide. Proc Natl Acad Sci U S A. 1976 Feb;73(2):462–466. doi: 10.1073/pnas.73.2.462. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. LOWRY O. H., ROSEBROUGH N. J., FARR A. L., RANDALL R. J. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265–275. [PubMed] [Google Scholar]
  20. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  21. Lagenaur C., Sommer I., Schachner M. Subclass of astroglia in mouse cerebellum recognized by monoclonal antibody. Dev Biol. 1980 Oct;79(2):367–378. doi: 10.1016/0012-1606(80)90122-0. [DOI] [PubMed] [Google Scholar]
  22. 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]
  23. Merril C. R., Switzer R. C., Van Keuren M. L. Trace polypeptides in cellular extracts and human body fluids detected by two-dimensional electrophoresis and a highly sensitive silver stain. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4335–4339. doi: 10.1073/pnas.76.9.4335. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. 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]
  25. Osborn M., Weber K. The detertent-resistant cytoskeleton of tissue culture cells includes the nucleus and the microfilament bundles. Exp Cell Res. 1977 May;106(2):339–349. doi: 10.1016/0014-4827(77)90179-3. [DOI] [PubMed] [Google Scholar]
  26. Pigott R., Kelly J. S. A cell surface antigen present on cultured cerebellar neurones appears to be transiently expressed during cerebellar development in the rat. Neurosci Lett. 1984 Aug 24;49(1-2):105–110. doi: 10.1016/0304-3940(84)90144-7. [DOI] [PubMed] [Google Scholar]
  27. Rougon G., Deagostini-Bazin H., Hirn M., Goridis C. Tissue- and developmental stage-specific forms of a neural cell surface antigen linked to differences in glycosylation of a common polypeptide. EMBO J. 1982;1(10):1239–1244. doi: 10.1002/j.1460-2075.1982.tb00019.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Rutishauser U. Developmental biology of a neural cell adhesion molecule. Nature. 1984 Aug 16;310(5978):549–554. doi: 10.1038/310549a0. [DOI] [PubMed] [Google Scholar]
  29. Rutishauser U., Edelman G. M. Effects of fasciculation on the outgrowth of neurites from spinal ganglia in culture. J Cell Biol. 1980 Nov;87(2 Pt 1):370–378. doi: 10.1083/jcb.87.2.370. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Rutishauser U., Gall W. E., Edelman G. M. Adhesion among neural cells of the chick embryo. IV. Role of the cell surface molecule CAM in the formation of neurite bundles in cultures of spinal ganglia. J Cell Biol. 1978 Nov;79(2 Pt 1):382–393. doi: 10.1083/jcb.79.2.382. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Rutishauser U., Thiery J. P., Brackenbury R., Edelman G. M. Adhesion among neural cells of the chick embryo. III. Relationship of the surface molecule CAM to cell adhesion and the development of histotypic patterns. J Cell Biol. 1978 Nov;79(2 Pt 1):371–381. doi: 10.1083/jcb.79.2.371. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Sadoul R., Hirn M., Deagostini-Bazin H., Rougon G., Goridis C. Adult and embryonic mouse neural cell adhesion molecules have different binding properties. 1983 Jul 28-Aug 3Nature. 304(5924):347–349. doi: 10.1038/304347a0. [DOI] [PubMed] [Google Scholar]
  33. Schachner M., Hedley-Whyte E. T., Hsu D. W., Schoonmaker G., Bignami A. Ultrastructural localization of glial fibrillary acidic protein in mouse cerebellum by immunoperoxidase labeling. J Cell Biol. 1977 Oct;75(1):67–73. doi: 10.1083/jcb.75.1.67. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Schnitzer J., Franke W. W., Schachner M. Immunocytochemical demonstration of vimentin in astrocytes and ependymal cells of developing and adult mouse nervous system. J Cell Biol. 1981 Aug;90(2):435–447. doi: 10.1083/jcb.90.2.435. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Schnitzer J., Schachner M. Developmental expression of cell type-specific markers in mouse cerebellar cells in vitro. J Neuroimmunol. 1981 Dec;1(4):471–487. doi: 10.1016/0165-5728(81)90024-2. [DOI] [PubMed] [Google Scholar]
  36. Schnitzer J., Schachner M. Expression of Thy-1, H-2, and NS-4 cell surface antigens and tetanus toxin receptors in early postnatal and adult mouse cerebellum. J Neuroimmunol. 1981 Dec;1(4):429–456. doi: 10.1016/0165-5728(81)90022-9. [DOI] [PubMed] [Google Scholar]
  37. Silver J., Rutishauser U. Guidance of optic axons in vivo by a preformed adhesive pathway on neuroepithelial endfeet. Dev Biol. 1984 Dec;106(2):485–499. doi: 10.1016/0012-1606(84)90248-3. [DOI] [PubMed] [Google Scholar]
  38. 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]
  39. Towbin H., Staehelin T., Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350–4354. doi: 10.1073/pnas.76.9.4350. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Webb M., Woodhams P. L. Monoclonal antibodies recognising cell surface molecules expressed by rat cerebellar interneurons. J Neuroimmunol. 1984 Jul;6(4):283–300. doi: 10.1016/0165-5728(84)90014-6. [DOI] [PubMed] [Google Scholar]
  41. Zanetta J. P., Roussel G., Ghandour M. S., Vincendon G., Gombos G. Postnatal development of rat cerebellum: massive and transient accumulation of concanavalin A binding glycoproteins in parallel fiber axolemma. Brain Res. 1978 Feb 24;142(2):301–319. doi: 10.1016/0006-8993(78)90637-6. [DOI] [PubMed] [Google Scholar]