Skip to main content
PMC home page
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1993 Jun 2;121(6):1409–1421. doi: 10.1083/jcb.121.6.1409

The fourth immunoglobulin-like domain of NCAM contains a carbohydrate recognition domain for oligomannosidic glycans implicated in association with L1 and neurite outgrowth

PMCID: PMC2119715  PMID: 8509458

Abstract

We have previously shown that the neural adhesion molecules L1 and NCAM interact with each other to form a complex which binds more avidly to L1 than L1 to L1 alone (Kadmon, G., A. Kowitz, P. Altevogt, and M. Schachner. 1990a. J. Cell Biol. 110:193-208). This cis-association between L1 and NCAM is carbohydrate-dependent (Kadmon, G., A. Kowitz, P. Altevogt, and M. Schachner. 1990b. J. Cell Biol. 110:209-218). In the present study, we report that L1 and NCAM bind to each other via oligomannosidic carbohydrates expressed by L1, but not by NCAM, as shown in several experiments: (a) complex formation between L1 and NCAM is inhibited by a mAb to oligomannosidic carbohydrates and by the oligosaccharides themselves; (b) NCAM binds to oligomannosidic carbohydrates; (c) within the L1/NCAM complex, the oligomannosidic carbohydrates are hidden from accessibility to a mAb against oligomannosidic carbohydrates; (d) the recombinant protein fragment of NCAM containing the immunoglobulin-like domains and not the fragment containing the fibronectin type III homologous repeats binds to oligomannosidic glycans. Furthermore, the fourth immunoglobulin-like domain of NCAM shows sequence homology with carbohydrate recognition domains of animal C-type lectins and, surprisingly, also with plant lectins. A peptide comprising part of the C-type lectin consensus sequence in the fourth immunoglobulin-like domain of NCAM interferes with the association between L1 and NCAM. The functional importance of oligomannosidic glycans at the cell surface was shown for neurite outgrowth in vitro. When neurons from early postnatal mouse cerebellum were maintained on laminin or poly-L-lysine, neurite outgrowth was inhibited by oligomannosidic glycans, by glycopeptides, glycoproteins, or neoglycolipids containing oligomannosidic glycans, but not by nonrelated oligosaccharides or oligosaccharide derivates. Neurite outgrowth was also inhibited by the peptide comprising part of the C- type lectin consensus sequence in the fourth immunoglobulin-like domain of NCAM. The combined results suggest that carbohydrate-mediated cis- associations between adhesion molecules at the cell surface modulate their functional properties.

Full Text

The Full Text of this article is available as a PDF (2.8 MB).

Selected References

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

  1. Antonicek H., Persohn E., Schachner M. Biochemical and functional characterization of a novel neuron-glia adhesion molecule that is involved in neuronal migration. J Cell Biol. 1987 Jun;104(6):1587–1595. doi: 10.1083/jcb.104.6.1587. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Arima T., Spiro M. J., Spiro R. G. Studies on the carbohydrate units of thyroglobulin. Evaluation of their microheterogeneity in the human and calf proteins. J Biol Chem. 1972 Mar 25;247(6):1825–1835. [PubMed] [Google Scholar]
  3. Barthels D., Santoni M. J., Wille W., Ruppert C., Chaix J. C., Hirsch M. R., Fontecilla-Camps J. C., Goridis C. Isolation and nucleotide sequence of mouse NCAM cDNA that codes for a Mr 79,000 polypeptide without a membrane-spanning region. EMBO J. 1987 Apr;6(4):907–914. doi: 10.1002/j.1460-2075.1987.tb04837.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Barton C. H., Dickson G., Gower H. J., Rowett L. H., Putt W., Elsom V., Moore S. E., Goridis C., Walsh F. S. Complete sequence and in vitro expression of a tissue-specific phosphatidylinositol-linked N-CAM isoform from skeletal muscle. Development. 1988 Sep;104(1):165–173. doi: 10.1242/dev.104.1.165. [DOI] [PubMed] [Google Scholar]
  5. Baumann C. M., Strosberg A. D., Rüdiger H. Purification and characterization of a mannose/glucose-specific lectin from Vicia cracca. Eur J Biochem. 1982 Feb;122(1):105–110. doi: 10.1111/j.1432-1033.1982.tb05854.x. [DOI] [PubMed] [Google Scholar]
  6. Bettler B., Hofstetter H., Rao M., Yokoyama W. M., Kilchherr F., Conrad D. H. Molecular structure and expression of the murine lymphocyte low-affinity receptor for IgE (Fc epsilon RII). Proc Natl Acad Sci U S A. 1989 Oct;86(19):7566–7570. doi: 10.1073/pnas.86.19.7566. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Bixby J. L., Jhabvala P. Extracellular matrix molecules and cell adhesion molecules induce neurites through different mechanisms. J Cell Biol. 1990 Dec;111(6 Pt 1):2725–2732. doi: 10.1083/jcb.111.6.2725. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Bixby J. L. Protein kinase C is involved in laminin stimulation of neurite outgrowth. Neuron. 1989 Sep;3(3):287–297. doi: 10.1016/0896-6273(89)90253-5. [DOI] [PubMed] [Google Scholar]
  9. Blithe D. L. N-linked oligosaccharides on free alpha interfere with its ability to combine with human chorionic gonadotropin-beta subunit. J Biol Chem. 1990 Dec 15;265(35):21951–21956. [PubMed] [Google Scholar]
  10. Bollensen E., Schachner M. The peripheral myelin glycoprotein P0 expresses the L2/HNK-1 and L3 carbohydrate structures shared by neural adhesion molecules. Neurosci Lett. 1987 Nov 10;82(1):77–82. doi: 10.1016/0304-3940(87)90174-1. [DOI] [PubMed] [Google Scholar]
  11. Bronner-Fraser M. Perturbation of cranial neural crest migration by the HNK-1 antibody. Dev Biol. 1987 Oct;123(2):321–331. doi: 10.1016/0012-1606(87)90390-3. [DOI] [PubMed] [Google Scholar]
  12. Cunningham B. A., Hemperly J. J., Murray B. A., Prediger E. A., Brackenbury R., Edelman G. M. Neural cell adhesion molecule: structure, immunoglobulin-like domains, cell surface modulation, and alternative RNA splicing. Science. 1987 May 15;236(4803):799–806. doi: 10.1126/science.3576199. [DOI] [PubMed] [Google Scholar]
  13. Devereux J., Haeberli P., Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387–395. doi: 10.1093/nar/12.1part1.387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Doege K., Sasaki M., Horigan E., Hassell J. R., Yamada Y. Complete primary structure of the rat cartilage proteoglycan core protein deduced from cDNA clones. J Biol Chem. 1987 Dec 25;262(36):17757–17767. [PubMed] [Google Scholar]
  15. Doherty P., Ashton S. V., Moore S. E., Walsh F. S. Morphoregulatory activities of NCAM and N-cadherin can be accounted for by G protein-dependent activation of L- and N-type neuronal Ca2+ channels. Cell. 1991 Oct 4;67(1):21–33. doi: 10.1016/0092-8674(91)90569-k. [DOI] [PubMed] [Google Scholar]
  16. Doherty P., Cohen J., Walsh F. S. Neurite outgrowth in response to transfected N-CAM changes during development and is modulated by polysialic acid. Neuron. 1990 Aug;5(2):209–219. doi: 10.1016/0896-6273(90)90310-c. [DOI] [PubMed] [Google Scholar]
  17. Doherty P., Moolenaar C. E., Ashton S. V., Michalides R. J., Walsh F. S. The VASE exon downregulates the neurite growth-promoting activity of NCAM 140. Nature. 1992 Apr 30;356(6372):791–793. doi: 10.1038/356791a0. [DOI] [PubMed] [Google Scholar]
  18. Dow K. E., Mirski S. E., Roder J. C., Riopelle R. J. Neuronal proteoglycans: biosynthesis and functional interaction with neurons in vitro. J Neurosci. 1988 Sep;8(9):3278–3289. doi: 10.1523/JNEUROSCI.08-09-03278.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Edelman G. M., Crossin K. L. Cell adhesion molecules: implications for a molecular histology. Annu Rev Biochem. 1991;60:155–190. doi: 10.1146/annurev.bi.60.070191.001103. [DOI] [PubMed] [Google Scholar]
  20. Fahrig Thomas, Schmitz Brigitte, Weber Dieter, Kücherer-Ehret Andrea, Faissner Andreas, Schachner Melitta. Two Monoclonal Antibodies Recognizing Carbohydrate Epitopes on Neural Adhesion Molecules Interfere with Cell Interactions. Eur J Neurosci. 1990 Feb;2(2):153–161. doi: 10.1111/j.1460-9568.1990.tb00407.x. [DOI] [PubMed] [Google Scholar]
  21. 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]
  22. Faissner A., Teplow D. B., Kübler D., Keilhauer G., Kinzel V., Schachner M. Biosynthesis and membrane topography of the neural cell adhesion molecule L1. EMBO J. 1985 Dec 1;4(12):3105–3113. doi: 10.1002/j.1460-2075.1985.tb04052.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Feizi T., Childs R. A. Carbohydrates as antigenic determinants of glycoproteins. Biochem J. 1987 Jul 1;245(1):1–11. doi: 10.1042/bj2450001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Fischer G., Künemund V., Schachner M. Neurite outgrowth patterns in cerebellar microexplant cultures are affected by antibodies to the cell surface glycoprotein L1. J Neurosci. 1986 Feb;6(2):605–612. doi: 10.1523/JNEUROSCI.06-02-00605.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Frei T., von Bohlen und Halbach F., Wille W., Schachner M. Different extracellular domains of the neural cell adhesion molecule (N-CAM) are involved in different functions. J Cell Biol. 1992 Jul;118(1):177–194. doi: 10.1083/jcb.118.1.177. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Gbarah A., Gahmberg C. G., Ofek I., Jacobi U., Sharon N. Identification of the leukocyte adhesion molecules CD11 and CD18 as receptors for type 1-fimbriated (mannose-specific) Escherichia coli. Infect Immun. 1991 Dec;59(12):4524–4530. doi: 10.1128/iai.59.12.4524-4530.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Geng J. G., Moore K. L., Johnson A. E., McEver R. P. Neutrophil recognition requires a Ca(2+)-induced conformational change in the lectin domain of GMP-140. J Biol Chem. 1991 Nov 25;266(33):22313–22318. [PubMed] [Google Scholar]
  28. Gloor S., Antonicek H., Sweadner K. J., Pagliusi S., Frank R., Moos M., Schachner M. The adhesion molecule on glia (AMOG) is a homologue of the beta subunit of the Na,K-ATPase. J Cell Biol. 1990 Jan;110(1):165–174. doi: 10.1083/jcb.110.1.165. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Hall H., Liu L., Schachner M., Schmitz B. The L2/HNK-1 carbohydrate mediates adhesion of neural cells to laminin. Eur J Neurosci. 1993 Jan 1;5(1):34–42. doi: 10.1111/j.1460-9568.1993.tb00202.x. [DOI] [PubMed] [Google Scholar]
  30. Hatton M. W., März L., Berry L. R., Debanne M. T., Regoeczi E. Bi-and tri-antennary human transferrin glycopeptides and their affinities for the hepatic lectin specific for asialo-glycoproteins. Biochem J. 1979 Sep 1;181(3):633–638. doi: 10.1042/bj1810633. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Hirn M., Pierres M., Deagostini-Bazin H., Hirsch M., Goridis C. Monoclonal antibody against cell surface glycoprotein of neurons. Brain Res. 1981 Jun 15;214(2):433–439. doi: 10.1016/0006-8993(81)91208-7. [DOI] [PubMed] [Google Scholar]
  32. 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]
  33. Hoyle G. W., Hill R. L. Structure of the gene for a carbohydrate-binding receptor unique to rat kupffer cells. J Biol Chem. 1991 Jan 25;266(3):1850–1857. [PubMed] [Google Scholar]
  34. Ji I., Ji T. H. Differential interactions of human choriogonadotropin and its antagonistic aglycosylated analog with their receptor. Proc Natl Acad Sci U S A. 1990 Jun;87(11):4396–4400. doi: 10.1073/pnas.87.11.4396. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Kadmon G., Kowitz A., Altevogt P., Schachner M. Functional cooperation between the neural adhesion molecules L1 and N-CAM is carbohydrate dependent. J Cell Biol. 1990 Jan;110(1):209–218. doi: 10.1083/jcb.110.1.209. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Kadmon G., Kowitz A., Altevogt P., Schachner M. The neural cell adhesion molecule N-CAM enhances L1-dependent cell-cell interactions. J Cell Biol. 1990 Jan;110(1):193–208. doi: 10.1083/jcb.110.1.193. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. 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]
  38. Kornfeld R., Kornfeld S. Assembly of asparagine-linked oligosaccharides. Annu Rev Biochem. 1985;54:631–664. doi: 10.1146/annurev.bi.54.070185.003215. [DOI] [PubMed] [Google Scholar]
  39. Krieg P. A., Sakaguchi D. S., Kintner C. R. Primary structure and developmental expression of a large cytoplasmic domain form of Xenopus laevis neural cell adhesion molecule (NCAM). Nucleic Acids Res. 1989 Dec 25;17(24):10321–10335. doi: 10.1093/nar/17.24.10321. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. 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]
  41. Krusius T., Gehlsen K. R., Ruoslahti E. A fibroblast chondroitin sulfate proteoglycan core protein contains lectin-like and growth factor-like sequences. J Biol Chem. 1987 Sep 25;262(27):13120–13125. [PubMed] [Google Scholar]
  42. Kücherer A., Faissner A., Schachner M. The novel carbohydrate epitope L3 is shared by some neural cell adhesion molecules. J Cell Biol. 1987 Jun;104(6):1597–1602. doi: 10.1083/jcb.104.6.1597. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. 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]
  44. Liang C. J., Yamashita K., Kobata A. Structural study of the carbohydrate moiety of bovine pancreatic ribonuclease B. J Biochem. 1980 Jul;88(1):51–58. [PubMed] [Google Scholar]
  45. Lipkin V. M., Khramtsov N. V., Andreeva S. G., Moshnyakov M. V., Petukhova G. V., Rakitina T. V., Feshchenko E. A., Ishchenko K. A., Mirzoeva S. F., Chernova M. N. Calmodulin-independent bovine brain adenylate cyclase. Amino acid sequence and nucleotide sequence of the corresponding cDNA. FEBS Lett. 1989 Aug 28;254(1-2):69–73. doi: 10.1016/0014-5793(89)81011-7. [DOI] [PubMed] [Google Scholar]
  46. 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]
  47. Martini R., Xin Y., Schmitz B., Schachner M. The L2/HNK-1 Carbohydrate Epitope is Involved in the Preferential Outgrowth of Motor Neurons on Ventral Roots and Motor Nerves. Eur J Neurosci. 1992;4(7):628–639. doi: 10.1111/j.1460-9568.1992.tb00171.x. [DOI] [PubMed] [Google Scholar]
  48. Matthew W. D., Reichardt L. F. Development and application of an efficient procedure for converting mouse IgM into small, active fragments. J Immunol Methods. 1982;50(3):239–253. doi: 10.1016/0022-1759(82)90162-4. [DOI] [PubMed] [Google Scholar]
  49. Pesheva P., Horwitz A. F., Schachner M. Integrin, the cell surface receptor for fibronectin and laminin, expresses the L2/HNK-1 and L3 carbohydrate structures shared by adhesion molecules. Neurosci Lett. 1987 Dec 29;83(3):303–306. doi: 10.1016/0304-3940(87)90104-2. [DOI] [PubMed] [Google Scholar]
  50. Pesheva P., Spiess E., Schachner M. J1-160 and J1-180 are oligodendrocyte-secreted nonpermissive substrates for cell adhesion. J Cell Biol. 1989 Oct;109(4 Pt 1):1765–1778. doi: 10.1083/jcb.109.4.1765. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Poltorak M., Sadoul R., Keilhauer G., Landa C., Fahrig T., Schachner M. Myelin-associated glycoprotein, a member of the L2/HNK-1 family of neural cell adhesion molecules, is involved in neuron-oligodendrocyte and oligodendrocyte-oligodendrocyte interaction. J Cell Biol. 1987 Oct;105(4):1893–1899. doi: 10.1083/jcb.105.4.1893. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. 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]
  53. 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]
  54. Santoni M. J., Goridis C., Fontecilla-Camps J. C. Molecular modelling of the immunoglobulin-like domains of the neural cell adhesion molecule (NCAM): implications for the positioning of functionally important sugar side chains. J Neurosci Res. 1988 Jul;20(3):304–310. doi: 10.1002/jnr.490200304. [DOI] [PubMed] [Google Scholar]
  55. Saukkonen K., Burnette W. N., Mar V. L., Masure H. R., Tuomanen E. I. Pertussis toxin has eukaryotic-like carbohydrate recognition domains. Proc Natl Acad Sci U S A. 1992 Jan 1;89(1):118–122. doi: 10.1073/pnas.89.1.118. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Schmalzing G., Kröner S., Schachner M., Gloor S. The adhesion molecule on glia (AMOG/beta 2) and alpha 1 subunits assemble to functional sodium pumps in Xenopus oocytes. J Biol Chem. 1992 Oct 5;267(28):20212–20216. [PubMed] [Google Scholar]
  57. 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]
  58. Sletten K., Kolberg J. The primary structure of the alpha chain of a mitogenic lectin from the seeds of Lathyrus sativus. Hoppe Seylers Z Physiol Chem. 1983 Aug;364(8):1047–1051. doi: 10.1515/bchm2.1983.364.2.1047. [DOI] [PubMed] [Google Scholar]
  59. Small S. J., Akeson R. Expression of the unique NCAM VASE exon is independently regulated in distinct tissues during development. J Cell Biol. 1990 Nov;111(5 Pt 1):2089–2096. doi: 10.1083/jcb.111.5.2089. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. 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]
  61. Stoll M. S., Mizuochi T., Childs R. A., Feizi T. Improved procedure for the construction of neoglycolipids having antigenic and lectin-binding activities, from reducing oligosaccharides. Biochem J. 1988 Dec 1;256(2):661–664. doi: 10.1042/bj2560661. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Streit A., Faissner A., Gehrig B., Schachner M. Isolation and biochemical characterization of a neural proteoglycan expressing the L5 carbohydrate epitope. J Neurochem. 1990 Nov;55(5):1494–1506. doi: 10.1111/j.1471-4159.1990.tb04931.x. [DOI] [PubMed] [Google Scholar]
  63. Tai T., Yamashita K., Kobata A. The substrate specificities of endo-beta-N-acetylglucosaminidases CII and H. Biochem Biophys Res Commun. 1977 Sep 9;78(1):434–441. doi: 10.1016/0006-291x(77)91273-6. [DOI] [PubMed] [Google Scholar]
  64. Taylor M. E., Bezouska K., Drickamer K. Contribution to ligand binding by multiple carbohydrate-recognition domains in the macrophage mannose receptor. J Biol Chem. 1992 Jan 25;267(3):1719–1726. [PubMed] [Google Scholar]
  65. Taylor M. E., Conary J. T., Lennartz M. R., Stahl P. D., Drickamer K. Primary structure of the mannose receptor contains multiple motifs resembling carbohydrate-recognition domains. J Biol Chem. 1990 Jul 25;265(21):12156–12162. [PubMed] [Google Scholar]
  66. Tomley F., Binns M., Campbell J., Boursnell M. Sequence analysis of an 11.2 kilobase, near-terminal, BamHI fragment of fowlpox virus. J Gen Virol. 1988 May;69(Pt 5):1025–1040. doi: 10.1099/0022-1317-69-5-1025. [DOI] [PubMed] [Google Scholar]
  67. Walsh F. S., Furness J., Moore S. E., Ashton S., Doherty P. Use of the neural cell adhesion molecule VASE exon by neurons is associated with a specific down-regulation of neural cell adhesion molecule-dependent neurite outgrowth in the developing cerebellum and hippocampus. J Neurochem. 1992 Nov;59(5):1959–1962. doi: 10.1111/j.1471-4159.1992.tb11033.x. [DOI] [PubMed] [Google Scholar]
  68. Weis W. I., Kahn R., Fourme R., Drickamer K., Hendrickson W. A. Structure of the calcium-dependent lectin domain from a rat mannose-binding protein determined by MAD phasing. Science. 1991 Dec 13;254(5038):1608–1615. doi: 10.1126/science.1721241. [DOI] [PubMed] [Google Scholar]
  69. Yang P., Yin X., Rutishauser U. Intercellular space is affected by the polysialic acid content of NCAM. J Cell Biol. 1992 Mar;116(6):1487–1496. doi: 10.1083/jcb.116.6.1487. [DOI] [PMC free article] [PubMed] [Google Scholar]
  70. Zhang H., Miller R. H., Rutishauser U. Polysialic acid is required for optimal growth of axons on a neuronal substrate. J Neurosci. 1992 Aug;12(8):3107–3114. doi: 10.1523/JNEUROSCI.12-08-03107.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES