Skip to main content
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1990 May 1;110(5):1729–1743. doi: 10.1083/jcb.110.5.1729

Olfactory neurons express a unique glycosylated form of the neural cell adhesion molecule (N-CAM)

PMCID: PMC2200194  PMID: 2186048

Abstract

mAb-based approaches were used to identify cell surface components involved in the development and function of the frog olfactory system. We describe here a 205-kD cell surface glycoprotein on olfactory receptor neurons that was detected with three mAbs: 9-OE, 5-OE, and 13- OE. mAb 9-OE immunoreactivity, unlike mAbs 5-OE and 13-OE, was restricted to only the axons and terminations of the primary sensory olfactory neurons in the frog nervous system. The 9-OE polypeptide(s) were immunoprecipitated and tested for cross-reactivity with known neural cell surface components including HNK-1, the cell adhesion molecule L1, and the neural cell adhesion molecule (N-CAM). These experiments revealed that 9-OE-reactive molecules were not L1 related but were a subset of the 200-kD isoforms of N-CAM. mAb 9-OE recognized epitopes associated with N-linked carbohydrate residues that were distinct from the polysialic acid chains present on the embryonic form of N-CAM. Moreover, 9-OE N-CAM was a heterogeneous population consisting of subsets both with and without the HNK-1 epitope. Thus, combined immunohistochemical and immunoprecipitation experiments have revealed a new glycosylated form of N-CAM unique to the olfactory system. The restricted spatial expression pattern of this N-CAM glycoform suggests a possible role in the unusual regenerative properties of this sensory system.

Full Text

The Full Text of this article is available as a PDF (3.8 MB).

Selected References

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

  1. Akeson R. A., Wujek J. R., Roe S., Warren S. L., Small S. J. Smooth muscle cells transiently express NCAM. Brain Res. 1988 Sep;464(2):107–120. doi: 10.1016/0169-328x(88)90003-4. [DOI] [PubMed] [Google Scholar]
  2. Akeson R., Seeger R. C. Interspecies neural membrane antigens on cultured human and murine neuroblastoma cells. J Immunol. 1977 Jun;118(6):1995–2003. [PubMed] [Google Scholar]
  3. Allen W. K., Akeson R. Identification of a cell surface glycoprotein family of olfactory receptor neurons with a monoclonal antibody. J Neurosci. 1985 Feb;5(2):284–296. doi: 10.1523/JNEUROSCI.05-02-00284.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Allen W. K., Akeson R. Identification of an olfactory receptor neuron subclass: cellular and molecular analysis during development. Dev Biol. 1985 Jun;109(2):393–401. doi: 10.1016/0012-1606(85)90465-8. [DOI] [PubMed] [Google Scholar]
  5. Chou D. K., Ilyas A. A., Evans J. E., Costello C., Quarles R. H., Jungalwala F. B. Structure of sulfated glucuronyl glycolipids in the nervous system reacting with HNK-1 antibody and some IgM paraproteins in neuropathy. J Biol Chem. 1986 Sep 5;261(25):11717–11725. [PubMed] [Google Scholar]
  6. 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]
  7. Dickson G., Gower H. J., Barton C. H., Prentice H. M., Elsom V. L., Moore S. E., Cox R. D., Quinn C., Putt W., Walsh F. S. Human muscle neural cell adhesion molecule (N-CAM): identification of a muscle-specific sequence in the extracellular domain. Cell. 1987 Sep 25;50(7):1119–1130. doi: 10.1016/0092-8674(87)90178-4. [DOI] [PubMed] [Google Scholar]
  8. Dodd J., Jessell T. M. Axon guidance and the patterning of neuronal projections in vertebrates. Science. 1988 Nov 4;242(4879):692–699. doi: 10.1126/science.3055291. [DOI] [PubMed] [Google Scholar]
  9. 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]
  10. Edelman G. M. Morphoregulatory molecules. Biochemistry. 1988 May 17;27(10):3533–3543. doi: 10.1021/bi00410a001. [DOI] [PubMed] [Google Scholar]
  11. Ezzell R. M., Kenney D. M., Egan S., Stossel T. P., Hartwig J. H. Localization of the domain of actin-binding protein that binds to membrane glycoprotein Ib and actin in human platelets. J Biol Chem. 1988 Sep 15;263(26):13303–13309. [PubMed] [Google Scholar]
  12. Goodman C. S., Bastiani M. J., Doe C. Q., du Lac S., Helfand S. L., Kuwada J. Y., Thomas J. B. Cell recognition during neuronal development. Science. 1984 Sep 21;225(4668):1271–1279. doi: 10.1126/science.6474176. [DOI] [PubMed] [Google Scholar]
  13. Gower H. J., Barton C. H., Elsom V. L., Thompson J., Moore S. E., Dickson G., Walsh F. S. Alternative splicing generates a secreted form of N-CAM in muscle and brain. Cell. 1988 Dec 23;55(6):955–964. doi: 10.1016/0092-8674(88)90241-3. [DOI] [PubMed] [Google Scholar]
  14. Graziadei G. A., Graziadei P. P. Neurogenesis and neuron regeneration in the olfactory system of mammals. II. Degeneration and reconstitution of the olfactory sensory neurons after axotomy. J Neurocytol. 1979 Apr;8(2):197–213. doi: 10.1007/BF01175561. [DOI] [PubMed] [Google Scholar]
  15. Graziadei P. P., Metcalf J. F. Autoradiographic and ultrastructural observations on the frog's olfactory mucosa. Z Zellforsch Mikrosk Anat. 1971;116(3):305–318. doi: 10.1007/BF00330630. [DOI] [PubMed] [Google Scholar]
  16. Harrelson A. L., Goodman C. S. Growth cone guidance in insects: fasciclin II is a member of the immunoglobulin superfamily. Science. 1988 Nov 4;242(4879):700–708. doi: 10.1126/science.3187519. [DOI] [PubMed] [Google Scholar]
  17. Hoffman S., Friedlander D. R., Chuong C. M., Grumet M., Edelman G. M. Differential contributions of Ng-CAM and N-CAM to cell adhesion in different neural regions. J Cell Biol. 1986 Jul;103(1):145–158. doi: 10.1083/jcb.103.1.145. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. 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]
  19. Hoffmann A. Stereotaxic atlas of the toad's brain. Acta Anat (Basel) 1973;84(3):416–451. doi: 10.1159/000143950. [DOI] [PubMed] [Google Scholar]
  20. Jacobson M., Rutishauser U. Induction of neural cell adhesion molecule (NCAM) in Xenopus embryos. Dev Biol. 1986 Aug;116(2):524–531. doi: 10.1016/0012-1606(86)90153-3. [DOI] [PubMed] [Google Scholar]
  21. Jessell T. M. Adhesion molecules and the hierarchy of neural development. Neuron. 1988 Mar;1(1):3–13. doi: 10.1016/0896-6273(88)90204-8. [DOI] [PubMed] [Google Scholar]
  22. Keller A., Margolis F. L. Immunological studies of the rat olfactory marker protein. J Neurochem. 1975 Jun;24(6):1101–1106. doi: 10.1111/j.1471-4159.1975.tb03883.x. [DOI] [PubMed] [Google Scholar]
  23. Key B., Giorgi P. P. Selective binding of soybean agglutinin to the olfactory system of Xenopus. Neuroscience. 1986 Jun;18(2):507–515. doi: 10.1016/0306-4522(86)90171-5. [DOI] [PubMed] [Google Scholar]
  24. Key B., Giorgi P. P. Soybean agglutinin binding to the olfactory systems of the rat and mouse. Neurosci Lett. 1986 Aug 29;69(2):131–136. doi: 10.1016/0304-3940(86)90591-4. [DOI] [PubMed] [Google Scholar]
  25. Kruse J., Mailhammer R., Wernecke H., Faissner A., Sommer I., Goridis C., Schachner M. Neural cell adhesion molecules and myelin-associated glycoprotein share a common carbohydrate moiety recognized by monoclonal antibodies L2 and HNK-1. Nature. 1984 Sep 13;311(5982):153–155. doi: 10.1038/311153a0. [DOI] [PubMed] [Google Scholar]
  26. Künemund V., Jungalwala F. B., Fischer G., Chou D. K., Keilhauer G., Schachner M. The L2/HNK-1 carbohydrate of neural cell adhesion molecules is involved in cell interactions. J Cell Biol. 1988 Jan;106(1):213–223. doi: 10.1083/jcb.106.1.213. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Levi G., Crossin K. L., Edelman G. M. Expression sequences and distribution of two primary cell adhesion molecules during embryonic development of Xenopus laevis. J Cell Biol. 1987 Nov;105(5):2359–2372. doi: 10.1083/jcb.105.5.2359. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Matsunaga M., Hatta K., Takeichi M. Role of N-cadherin cell adhesion molecules in the histogenesis of neural retina. Neuron. 1988 Jun;1(4):289–295. doi: 10.1016/0896-6273(88)90077-3. [DOI] [PubMed] [Google Scholar]
  29. Miragall F., Kadmon G., Husmann M., Schachner M. Expression of cell adhesion molecules in the olfactory system of the adult mouse: presence of the embryonic form of N-CAM. Dev Biol. 1988 Oct;129(2):516–531. doi: 10.1016/0012-1606(88)90397-1. [DOI] [PubMed] [Google Scholar]
  30. Parekh R. B., Tse A. G., Dwek R. A., Williams A. F., Rademacher T. W. Tissue-specific N-glycosylation, site-specific oligosaccharide patterns and lentil lectin recognition of rat Thy-1. EMBO J. 1987 May;6(5):1233–1244. doi: 10.1002/j.1460-2075.1987.tb02359.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Plenderleith M. B., Cameron A. A., Key B., Snow P. J. Soybean agglutinin binds to a subpopulation of primary sensory neurones in the cat. Neurosci Lett. 1988 Apr 12;86(3):257–262. doi: 10.1016/0304-3940(88)90492-2. [DOI] [PubMed] [Google Scholar]
  32. Plenderleith M. B., Cameron A. A., Key B., Snow P. J. The plant lectin soybean agglutinin binds to the soma, axon and central terminals of a subpopulation of small-diameter primary sensory neurons in the rat and cat. Neuroscience. 1989;31(3):683–695. doi: 10.1016/0306-4522(89)90433-8. [DOI] [PubMed] [Google Scholar]
  33. Prediger E. A., Hoffman S., Edelman G. M., Cunningham B. A. Four exons encode a 93-base-pair insert in three neural cell adhesion molecule mRNAs specific for chicken heart and skeletal muscle. Proc Natl Acad Sci U S A. 1988 Dec;85(24):9616–9620. doi: 10.1073/pnas.85.24.9616. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Prince J. T., Milona N., Stallcup W. B. Characterization of a partial cDNA clone for the NILE glycoprotein and identification of the encoded polypeptide domain. J Neurosci. 1989 May;9(5):1825–1834. doi: 10.1523/JNEUROSCI.09-05-01825.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Rademacher T. W., Parekh R. B., Dwek R. A. Glycobiology. Annu Rev Biochem. 1988;57:785–838. doi: 10.1146/annurev.bi.57.070188.004033. [DOI] [PubMed] [Google Scholar]
  36. 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]
  37. Rutishauser U., Acheson A., Hall A. K., Mann D. M., Sunshine J. The neural cell adhesion molecule (NCAM) as a regulator of cell-cell interactions. Science. 1988 Apr 1;240(4848):53–57. doi: 10.1126/science.3281256. [DOI] [PubMed] [Google Scholar]
  38. Santoni M. J., Barthels D., Vopper G., Boned A., Goridis C., Wille W. Differential exon usage involving an unusual splicing mechanism generates at least eight types of NCAM cDNA in mouse brain. EMBO J. 1989 Feb;8(2):385–392. doi: 10.1002/j.1460-2075.1989.tb03389.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Small S. J., Haines S. L., Akeson R. A. Polypeptide variation in an N-CAM extracellular immunoglobulin-like fold is developmentally regulated through alternative splicing. Neuron. 1988 Dec;1(10):1007–1017. doi: 10.1016/0896-6273(88)90158-4. [DOI] [PubMed] [Google Scholar]
  40. Small S. J., Shull G. E., Santoni M. J., Akeson R. Identification of a cDNA clone that contains the complete coding sequence for a 140-kD rat NCAM polypeptide. J Cell Biol. 1987 Nov;105(5):2335–2345. doi: 10.1083/jcb.105.5.2335. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Stallcup W. B., Beasley L. L., Levine J. M. Antibody against nerve growth factor-inducible large external (NILE) glycoprotein labels nerve fiber tracts in the developing rat nervous system. J Neurosci. 1985 Apr;5(4):1090–1101. doi: 10.1523/JNEUROSCI.05-04-01090.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Sunshine J., Balak K., Rutishauser U., Jacobson M. Changes in neural cell adhesion molecule (NCAM) structure during vertebrate neural development. Proc Natl Acad Sci U S A. 1987 Aug;84(16):5986–5990. doi: 10.1073/pnas.84.16.5986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Walsh F. S., Parekh R. B., Moore S. E., Dickson G., Barton C. H., Gower H. J., Dwek R. A., Rademacher T. W. Tissue specific O-linked glycosylation of the neural cell adhesion molecule (N-CAM). Development. 1989 Apr;105(4):803–811. doi: 10.1242/dev.105.4.803. [DOI] [PubMed] [Google Scholar]
  44. Williams R. K., Goridis C., Akeson R. Individual neural cell types express immunologically distinct N-CAM forms. J Cell Biol. 1985 Jul;101(1):36–42. doi: 10.1083/jcb.101.1.36. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES