Carbohydrate Recognition, Cell Interactions, and Vertebrate Neural Development

  • M. A. Hynes
  • J. Dodd
  • T. M. Jessell


The formation of selective connections between distinct subsets of neurons is a critical step in the generation of functional neural circuits. During embryogenesis, several sequential steps contribute to the final pattern of neural connectivity. First, the differential adhesive properties of neural and nonneural epithelial cells result in the segregation and shaping of early neural tissues. The establishment of basic morphological features is accompanied by the migration of neuroblasts and their differentiation into distinct subsets of neurons. The axons of differentiated neurons then project to their prospective cellular targets under the influence of a series of diffusible cell surface and matrix-associated guidance cues. Axonal growth cones then appear to recognize and select appropriate cellular targets with which to form stable contacts. Each of these developmental steps is dependent on a precisely coordinated program of intercellular recognition.


Neural Cell Adhesion Molecule High Endothelial Venule Tectal Membrane Carbohydrate Binding Protein Lymphocyte Homing 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Andrews, P., Milsom, D. W., and Stoddart, R. W., 1983, Glycoconjugates from high endothelial cells. I. Partial characterization of a sulphated glycoconjugate from the high endothelial cells of rat lymph nodes, J. Cell Sci. 59: 231–244.PubMedGoogle Scholar
  2. Ariga, T., Kohriyama, T., Freddo, L., Latov, N., Saito, M., Kon, K., Ando, S., Suzuki, M., Hemling, M. E., Rinehart, K. L., Kusunoki, S., and Yu, R. K., 1987, Characterization of sulfated glucuronic acid containing glycolipids reacting with IgM proteins in patients with neuropathy. J. Biol. Chem. 262: 848–854.PubMedGoogle Scholar
  3. Ashwell, G., and Harford, J., 1982, Carbohydrate-specific receptors of the liver, Annu. Rev. Biochem. 51: 531–554.PubMedCrossRefGoogle Scholar
  4. Balsamo, J., Pratt, R. S., and Lilien, J., 1986, Chick neural retina N-acetylgalactosaminyltransferase/acceptor complex: Catalysis involves transfer of N-acetylgalactosamine phosphate to endogenous acceptors, Biochemistry 25: 5402–5407.PubMedCrossRefGoogle Scholar
  5. Barbera, A. J., 1975, Adhesive recognition between developing retinal cells and the optic-tecta of the chick embryo, Dev. Biol. 46: 167–191.PubMedCrossRefGoogle Scholar
  6. Barbera, A. J., Marchase, R. B., and Roth, S., 1973, Adhesive recognition and retinotectal specificity, Proc. Natl. Acad. Sci. USA 70: 2482–2486.PubMedCrossRefGoogle Scholar
  7. Barondes, S. H., 1970, Brain glycomacromolecules and interneuronal recognition, in: Neurosciences: Second Study Program ( F. O. Schmitt, ed.), pp. 747–760, Rockefeller University Press, New York.Google Scholar
  8. Barondes, S. H., 1984, Soluble lectins: A new class of extracellular proteins, Science 233: 1259–1264.CrossRefGoogle Scholar
  9. Barondes, S. H., and Haywood-Reid, P. L., 1981, Externalization of an endogenous chicken muscle lectin with in vivo development, J. Cell Biol. 91: 568–572.PubMedCrossRefGoogle Scholar
  10. Bayna, E. M., Runyan, R. B., Scully, N. F., Reichner, J., Lopez, L. C., and Shur, B. D., 1986, Cell surface galactosyltransferase as a recognition molecule during development, Mol. Cell. Biochem. 72: 141–151.PubMedCrossRefGoogle Scholar
  11. Bayna, E. M., Shaper, J. H., and Shur, B. D., 1988, Temporally specific involvement of cell surface ß-1,4 galactosyltransferase during mouse embryo morula compaction, Cell 53: 145–157.PubMedCrossRefGoogle Scholar
  12. Beyer, E. C., and Barondes, S. H., 1982, Secretion of endogenous lectin by chicken intestinal goblet cells, J. Cell Biol. 92: 28–33.PubMedCrossRefGoogle Scholar
  13. Blackburn, C. C., Swank-Hill, P., and Schnarr, R. L., 1986, Gangliosides support neural retina cell adhesion, J. Biol. Chem. 261: 2873–2881.PubMedGoogle Scholar
  14. Bleil, J. D., and Wassarman, P. M., 1988, Galactose at the nonreducing terminus of 0-linked oligosaccharides of mouse egg ZP3 is essential for the glycoprotein’s sperm receptor activity, Proc. Natl. Acad. Sci. USA 85 (18): 6778–6782.PubMedCrossRefGoogle Scholar
  15. Blum, A. S., and Barnstable, C. J., 1987, 0-acetylation of a cell-surface carbohydrate creates discrete molecular patterns during neural development, Proc. Natl. Acad. Sci. USA 84: 8716–8720.Google Scholar
  16. Bollensen, E., and Schachner, M., 1987, The peripheral myelin glycoprotein PO expresses the L2/HNK-1 and L3 carbohydrate structures shared by neural adhesion molecules, Neurosci. Lett. 82: 77–82.PubMedCrossRefGoogle Scholar
  17. Bols, N. C., Roberson, M. M., Haywood-Reid, P. L., Cerra, R. F., and Barondes, S. H., 1986, Secretion of a cytoplasmic lectin from Xenopus laevis skin, J. Cell Biol. 102: 492–499.PubMedCrossRefGoogle Scholar
  18. Bonhoeffer, F., and Huf, J., 1982, In vitro experiments on axon guidance demonstrating an anterior—posterior gradient on the tectum, EMBO J. 1: 427–431.Google Scholar
  19. Bonhoeffer, F., and Huf, J., 1984, Position-dependent properties of retinal axons and their growth cones, Nature 315: 409–410.CrossRefGoogle Scholar
  20. Brandley, B. K., Ross, T. S., and Schnarr, R. L., 1987, Multiple carbohydrate receptors on lymphocytes revealed by adhesion to immobilized polysaccharides, J. Cell Biol. 105: 991–997.PubMedCrossRefGoogle Scholar
  21. Brown, A. G., 1981, Organization in the Spinal Cord, p. 239, Springer-Verlag, Berlin.Google Scholar
  22. Calarco-Gillam, P., 1985, Cell—cell interactions in mammalian preimplantation development, in: Developmental Biology: A Comprehensive Synthesis, Vol. 2 ( L. Browder, ed.), pp. 329–371, Plenum Press, New York.Google Scholar
  23. Cena, R. F., Haywood-Reid, P. L., and Barondes, S. H., 1984, Endogenous mammalian lectin localized extracellularly in lung elastic fibers, J. Cell Biol. 98: 1580–1589.CrossRefGoogle Scholar
  24. Cena, R. F., Gitt, M. A., and Barondes, S. H., 1985, Three soluble rat (3-galactoside-binding lectins, J. Biol. Chem. 260: 10474–10477.Google Scholar
  25. Chiacchia, K. B., and Drickamer, K., 1984, Direct evidence for the transmembrane orientation of the hepatic glycoprotein receptors, J. Biol. Chem. 259: 15440–15446.PubMedGoogle Scholar
  26. Childs, R. A., and Feizi, T., 1979, Calf heart lectin reacts with blood group Ii antigens and other precursor chains of the major blood group antigens, FEBS Lett. 99: 175–179.PubMedCrossRefGoogle Scholar
  27. Chou, D. K., Ilyas, A. A., Evans, J. E., Costello, C., Quarles, R. H., and Jungalwala, F. B., 1986, Structure of sulfated glucuronyl glycolipids in the nervous system reacting with HNK-1 antibody and some IgM paraproteins in neuropathy, J. Biol. Chem. 261: 11717–11725.PubMedGoogle Scholar
  28. Clerch, L. B., Whitney, P., Hass, M., Brew, K., Miller, T., Werner, R., and Massaro, D., 1988, Sequence of a full-length cDNA for rat lung 3-galactoside-binding protein: Primary and secondary structure of the lectin, Biochemistry 27: 692–699.PubMedCrossRefGoogle Scholar
  29. Cole, G. J., and Schachner, M., 1987, Localization of the L2 monoclonal antibody binding site on N-CAM and evidence for its role in N-CAM mediated cell adhesion, Neurosci. Lett. 78: 227–232.PubMedCrossRefGoogle Scholar
  30. DeWaard, A., Hickman, S., and Kornfeld, S., 1976, Isolation and properties of ß-galactoside-binding lectins of calf heart and lung, J. Biol. Chem. 251: 7581–7587.Google Scholar
  31. Dodd, J., and Jessell, T. M., 1985, Lactoseries carbohydrates specify subsets of dorsal root ganglion neurons projecting to superficial dorsal horn of rat spinal cord, J. Neurosci. 5: 3278–3294.PubMedGoogle Scholar
  32. Dodd, J., and Jessell, T. M., 1986, Cell surface glycoconjugates and carbohydrate-binding proteins: Possible recognition signals in sensory neurone development, J. Exp. Biol. 129: 225–238.Google Scholar
  33. Dodd, J., Solter, D., and Jessell, T. M., 1984, Monoclonal antibodies against carbohydrate differentiation antigens identify subsets of primary sensory neurons, Nature 311: 469–472.PubMedCrossRefGoogle Scholar
  34. Dodd, J.,Morton, S. B., Karagogeos, D., Yamamoto, M., and Jessell, T. M., 1988, Spatial regulation of axonal glycoprotein expression on subsets of embryonic spinal neurons, Neuron 1(2):105–116.Google Scholar
  35. Drickamer, K., 1987, Membrane receptors that mediate glycoprotein endocytosis: Structure and biosynthesis, Kidney Int. 32: 5167 — S183.Google Scholar
  36. Drickamer, K., 1988, Two distinct classes of carbohydrate-recognition domains in animal lectins, J. Biol. Chem. 263: 9557–9560.PubMedGoogle Scholar
  37. Dubois, C., Magnani, J. L., Grunwald, G. B., Spitalnik, S. L., Trisler, G. D., Nirenberg, M., and Ginsburg, V., 1986, Monoclonal antibody 18B8, which detects synapse-associated antigens, binds to ganglioside GT3 (II3(NeuAc)3 LacCer), J. Biol. Chem. 261: 3826–3830.PubMedGoogle Scholar
  38. Edelman, G. M., 1986, Cell adhesion molecules in the regulation of animal form and tissue pattern, Annu. Rev. Cell Biol. 2: 81–116.PubMedCrossRefGoogle Scholar
  39. Edelman, G. M., Murray, B. A., Mege, R. M., Cunningham, B. A., and Gallin, W. A., 1987, Cellular expression of liver and neural cell adhesion molecules after trantfection with their cDNAs results in specific cell—cell binding, Proc. Natl. Acad. Sci. USA 84: 8502–8506.PubMedCrossRefGoogle Scholar
  40. Eisenbarth, G. S., Ruffolo, R. R., Walsh, F. S., and Nirenberg, M., 1978, Lactose sensitive lectin of chick retina and spinal cord, Biochem. Biophys. Res. Commun. 83: 1246–1252.PubMedCrossRefGoogle Scholar
  41. Fenderson, B. A., Zehavi, U., and Hakomori, S. I., 1984, A multivalent lacto-N-fucopentose III-lysyllysine conjugate decompacts preimplantation mouse embryos, while the free oligo-saccharide is ineffective, J. Exp. Med. 160: 1591–1596.PubMedCrossRefGoogle Scholar
  42. Gallatin, M., St. John, T. P., Siegelman, M., Reichert, R., Butcher, E. C., and Weissman, I. L., 1986, Lymphocyte homing receptors, Cell 44: 673–680.PubMedCrossRefGoogle Scholar
  43. Gesner, B. M., and Ginsberg, V., 1964, Effect of glycosidases on the fate of transfused lymphocytes, Proc. Natl. Acad. Sci. USA 52: 750–755.PubMedCrossRefGoogle Scholar
  44. Gitt, M. A., and Barondes, S. H., 1986, Evidence that a human soluble 3-galactoside-binding lectin is encoded by a family of genes, Proc. Natl. Acad. Sci. USA 83: 7603–7607.PubMedCrossRefGoogle Scholar
  45. Glabe, C. G., Grabel, L. B., Vacquier, V. D., and Rosen, S. D., 1982, Carbohydrate specificity of sea urchin sperm bindin: A cell surface lectin mediating sperm—egg adhesion, J. Cell Biol. 94: 123–128.PubMedCrossRefGoogle Scholar
  46. Gobel, S., Falls, W. M., and Humphrey, E., 1981, Morphology and synaptic connections of ultrafine primary axons in lamina 1 of the spinal dorsal horn: Candidates for the terminal axonal arbors of primary neurons with unmyelinated axons, J. Neurosci. 1: 1163–1179.PubMedGoogle Scholar
  47. Grabel, L. B., 1984, Isolation of a putative cell adhesion mediating lectin from teratocarcinoma stem cells and its possible role in differentiation, Cell Differ. 15:121–124.Google Scholar
  48. Grabel, L. B., Singer, M. S., Rosen, S. D., and Martin, G. R., 1983, The role of carbohydrates in the intercellular adhesion and differentiation of teratocarcinoma stem cells, in: Teratocarcinoma Stem Cells, Vol. 10 ( L. M. Silver, G. R. Martin, and S. Strickland, eds.), pp. 145–163, Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.Google Scholar
  49. Grabel, L. B., Singer, M. S., Martin, G. R., and Rosen, S. D., 1985, Isolation of a teratocarcinoma stem cell lectin implicated in intercellular adhesion, FEBS Lett. 183 (2): 228–231.PubMedCrossRefGoogle Scholar
  50. Grunwald, G. B., Fredman, P., Magnani, J. L., Trisler, D., Ginsburg, V., and Nirenberg, M., 1985, Monoclonal antibody 18B8 detects gangliosides associated with neuronal differentiation and synapse formation, Proc. Natl. Acad. Sci. USA 82: 4008–4012.PubMedCrossRefGoogle Scholar
  51. Haagsman, H. P., Haegood, S., Sargeant, I., Buckley, D., White, R. T., Drickamer, K., and Benison, B. J., 1987, The major lung surfactant protein, SP 28–36, is a calcium-dependent, carbohydrate-binding protein, J. Biol. Chem. 262: 13877–13880.PubMedGoogle Scholar
  52. Hakomori, S., 1981, Glycosphingolipids in cellular interaction, differentiation and oncogenesis, Annu. Rev. Biochem. 50: 733–764.PubMedCrossRefGoogle Scholar
  53. Halberg, D. F., Proulx, G., Doege, K., Yamada, Y., and Drickamer, K., 1988, A segment of the cartilage proteoglycan core protein has lectin-like properties, J. Biol. Chem. 263: 9486–9490.PubMedGoogle Scholar
  54. Halfter, W., Claviez, M., and Schwarz, U., 1981, Preferential adhesion of tectal membranes to anterior embryonic chick retina neurites, Nature 292: 67–70.PubMedCrossRefGoogle Scholar
  55. Hinek, A., Wrenn, D. S., Mecham, R. P., and Barondes, S. H., 1988, The elastin receptor is a galactoside binding protein, Science 239: 6159.CrossRefGoogle Scholar
  56. Huang, T., and Yanagimachi, R., 1984, Fucoidin inhibits attachment of guinea pig spermatozoa to the zona pellucida through binding to the inner acrosomal membrane and equitonal domains, Exp. Cell Res. 153: 363–373.PubMedCrossRefGoogle Scholar
  57. Hyafil, F., Morello, D., Babinet, C., and Jacob, F., 1980, A cell surface glycoprotein involved in the compaction of embryonal carcinoma cells and cleavage stage embryos, Cell 21: 927–934.PubMedCrossRefGoogle Scholar
  58. Hynes, M. A., Buck, L. B., Casano, F. I., Huang, K. K., Barondes, S. H., and Jessell, T. M., 1988, Cloning and expression of a soluble 14 kDa 3-galactoside binding lectin in rat nervous system, Soc. Neurosci. Abstr. 14: 71.Google Scholar
  59. Jessell, T. M., 1988, Adhesion molecules and the hierarchy of neural development, Neuron 1: 3–13.PubMedCrossRefGoogle Scholar
  60. Jessell, T. M., and Dodd, J., 1985, Structure and expression of differentiation antigens on functional subclasses of primary sensory neurons, Philos. Trans. R. Soc. London Ser. B 308: 271–281.CrossRefGoogle Scholar
  61. Jia, S., and Wang, J. J., 1988, Carbohydrate binding protein 35: Complementary DNA sequence reveals homology with proteins of the hnRNP, J. Biol. Chem. 263: 6009–6011.PubMedGoogle Scholar
  62. Kobiler, D., and Barondes, S. H., 1977, Lectin activity from embryonic chick brain, heart and liver: Changes with development, Dey. Biol. 60: 326–330.CrossRefGoogle Scholar
  63. Kobiler, D., Beyer, E. C., and Barondes, S. H., 1978, Developmentally regulated lectins from chick muscle, brain and liver have similar chemical and immunological properties, Dey. Biol. 64: 265–272.CrossRefGoogle Scholar
  64. Krantz, M. J., Holtman, N., Stowell, C., and Lee, Y. C., 1976, Attachment of thioglycosides to proteins: Enhancement of liver membrane binding, Biochemistry 15: 3963.PubMedCrossRefGoogle Scholar
  65. Kruse, J., Mallhammer, R., Weinecke, H., Falssner, A., Sommer, I., Goridis, C., and Schachner, M., 1984, Neural cell adhesion molecules and myeline-associated glycoprotein share a common carbohydrate moiety recognized by monoclonal antibodies L2 and HNK-1, Nature 311: 153–155.PubMedCrossRefGoogle Scholar
  66. Kruse, J., Keilhauer, G., Falssner, A., Timpl, R., and Schachner, M., 1985, The J1 glycoprotein—A novel nervous system cell adhesion molecule of the L2/HNK-1 family, Nature 316: 146–148.PubMedCrossRefGoogle Scholar
  67. Krusius, T., Gehlsen, K. R., and Ruoslahti, E., 1987, A fibroblast chondroitin sulfate proteoglycan core protein contains lectin-like and growth factor-like sequences, J. Biol. Chem. 262: 13120–13125.PubMedGoogle Scholar
  68. Kucherer, A., Faissner, A., and Schachner, M., 1987, The novel carbohydrate epitope L3 is shared by some neural cell adhesion molecules, J. Cell Biol. 104: 1597–1602.PubMedCrossRefGoogle Scholar
  69. Kuhlenschmidt, T. B., Kuhlenschmidt, M. S., Roseman, S., and Lee, Y. C., 1984, Binding and endocytosis of glycoproteins by isolated chicken hepatocytes, Biochemistry 23: 6437–6444.PubMedCrossRefGoogle Scholar
  70. Kunemund, V., Jungalwala, F. B., Fischer, G., Chou, D. K. H., Keilhauer, G., and Schachner, M., 1988, The L2/HNK-1 carbohydrate of neural cell adhesion molecules is involved in cell interactions, J. Cell Biol. 106:213–223.Google Scholar
  71. Lagenaur, C., and Lemmon, V., 1987, An L1-like molecule, the 8D9 antigen, is a potent substrate for neurite extension, Proc. Natl. Acad. Sci. USA 84: 7753–7757.PubMedCrossRefGoogle Scholar
  72. Leffler, H., and Barondes, S. H., 1986, Specificity of binding of three soluble rat lung lectins to substituted and unsubstituted mammalian ß-galactosides, J. Biol. Chem. 261: 10119–10126.PubMedGoogle Scholar
  73. Levine, J. M., Beasley, L., and Stallcup, W. B., 1984, the D1.1 antigen: A cell surface marker for germinal cells of the central nervous system, J. Neurosci. 4: 820–831.Google Scholar
  74. Lopez, L. C., Bayna, E. M., Litoff, D., Shaper, N. L., and Shur, B. D., 1985, Receptor function of mouse sperm surface galactosyltransferase during fertilization, J. Cell Biol. 101: 1501–1510.PubMedCrossRefGoogle Scholar
  75. Marchase, R. B., 1977, Biochemical investigations of retinotectal adhesive specificity, J. Cell Biol. 75: 237–257.PubMedCrossRefGoogle Scholar
  76. McGarry, R. C., Riopelle, R. J., and Roder, J. C., 1985, Accelerated regenerative neurite formation by a neuronal surface epitope reactive with the monoclonal antibody, Leu 7, Neurosci. Leu. 56: 95–100.CrossRefGoogle Scholar
  77. Nagafuchi, A., Shirayoshi, Y., Okazaki, K., Yasuda, K., and Takeichi, M., 1987, Transformation of cell adhesion properties by exogenously introduced E-cadherin cDNA, Nature 329: 341–343.PubMedCrossRefGoogle Scholar
  78. Narimatsu, H., Sinha, S., Brew, K., Okayama, H., and Qasba, P. K., 1986, Cloning and sequencing of cDNA of bovine N-acetylglucosamine (31–4) galactosyltransferase, Proc. Natl. Acad. Sci. USA 83: 4720–4724.PubMedCrossRefGoogle Scholar
  79. Obata, K., Oide, M., and Handa, S., 1977, Effects of glycolipids on in vitro development of neuromuscular junction, Nature 266: 369–371.PubMedCrossRefGoogle Scholar
  80. Paroutaud, P., Levi, G., Teichberg, V. I., and Strosberg, A. D., 1987, Extensive amino acid sequence homologies between animal lectins, Proc. Natl. Acad. Sci. USA 84: 6345–6348.PubMedCrossRefGoogle Scholar
  81. Pesheva, P., Horwitz, A. F., and Schachner, M., 1987, Integrin, the cell surface receptor for fibronectin and laminin, expresses the L2/HNK-1 and L3 carbohydrate structures shared by adhesion molecules, Neurosci. Leu. 83: 303–306.CrossRefGoogle Scholar
  82. Poltorak, M., Sadoul, R., Keilhauer, G., Landa, C., and Schachner, M., 1987, The myelin-associated glycoprotein (MAG), 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. 105: 1893 1899.Google Scholar
  83. Rastan, S., Thorpe, S. J., Scudder, D. P., Brown, S., Gooi, H. C., and Feizi, T., 1985, Cell interactions in preimplantation embryos: Evidence for involvement of saccharides of the poly-N-acetyllactosamine series, J. Embryol. Exp. Morphol. 87: 115–128.Google Scholar
  84. Regan, L., Dodd, J., Barondes, S. H., and Jessell, T. M., 1986, Selective expression of endogenous lactose-binding lectins and lactoseries glycoconjugates in subsets of rat sensory neurons, Proc. Natl. Acad. Sci. USA 83: 2248–2252.PubMedCrossRefGoogle Scholar
  85. Rethelyi, M., 1977, Preterminal and terminal arborizations within substantia gelatinosa of cat spinal cord, J. Comp. Neurol. 172: 511–528.PubMedCrossRefGoogle Scholar
  86. Riopelle, R. J., McGarry, R. C., and Roder, J. C., 1986, Adhesion properties of a neuronal epitope recognized by the monoclonal antibody HNK-1, Brain Res. 367: 20–25.Google Scholar
  87. Roseman, S., 1970, The synthesis of complex carbohydrates by multiglycosyltransferase systems and their potential function in intercellular adhesion, Chem. Phys. Lip. 5: 270–297.CrossRefGoogle Scholar
  88. Rosen, S. D., and Yednock, T. A., 1986, Lymphocyte attachment to high endothelial venules during recirculation: A possible role for carbohydrates as recognition determinants, Mol. Cell. Biochem. 72: 153–164.PubMedCrossRefGoogle Scholar
  89. Rosen, S. D., Singer, M. S., Yednock, T. A., and Stoolman, L. M., 1985, Involvement of sialic acid on endothelial cells in organ-specific lymphocyte recirculation, Science 228: 1005–1007.PubMedCrossRefGoogle Scholar
  90. Roth, S., McGuire, E. J., and Roseman, J., 1971, Evidence for cell-surface glycosyltransferases: Their potential role in cellular recognition, J. Cell Biol. 51: 526–547.Google Scholar
  91. Rutishauser, U., and Jessell, T. M., 1988, Cell adhesion molecules in vertebrate neural development, in: Physiological Reviews, The American Physiological Society, Bethesda, 68 (3): 819–857.Google Scholar
  92. Rutishauser, U., and Goridis, C., 1986, N-CAM: The molecule and its genetics, Trends Genet. 2: 72–76.CrossRefGoogle Scholar
  93. Sanes, J. R., and Cheney, M., 1982, Lectin binding reveals a synapse specific carbohydrate in skeletal muscle, Nature 300: 646–647.PubMedCrossRefGoogle Scholar
  94. Schachner, M., Faissner, A., Fischer, G., Keilhauer, G., Kruse, J., Kunemund, V., Linder, J., and Wemecke, H., 1985, Functional and structural aspects of the cell surface in mammalian nervous system development, in: The Cell in Contact ( G. M. Edelman and J. P. Thiery, eds.), pp. 257–275, Wiley, New York.Google Scholar
  95. Scott, L. J. C., Bacon, F., and Sanes, J. R., 1988, A synapse-specific carbohydrate of the neuromuscular junction: Association with both acetylcholinesterase and a glycolipid, J. Neurosci. 8: 932–944.PubMedGoogle Scholar
  96. Shaper, N. L., Shaper, J. H., Meuth, J. L., Fox, J. L., Chang, H., Kirsch, I. R., and Hollis, G. F., 1986, Bovine galactosyltransferase: Identification of a clone by direct immunological screening of a cDNA expression library, Proc. Natl. Acad. Sci. USA 83: 1573–1577.PubMedCrossRefGoogle Scholar
  97. Shur, B. C., 1983, Embryonal carcinoma cell adhesion: The role of surface galactosyltransferase and its 90K lactosaminoglycan substrate, Dev. Biol. 99: 360–372.PubMedCrossRefGoogle Scholar
  98. Sly, W. S., and Fischer, H. D., 1982, The phosphomannosyl recognition system for intracellular and intercellular transport of lysosomal enzymes, J. Cell Biochem. 18: 67–85.PubMedCrossRefGoogle Scholar
  99. Smith, C. S., 1983, The development and postnatal organization of primary afferent projections to the rat thoracic spinal cord, J. Comp. Neurol. 220: 29–43.PubMedCrossRefGoogle Scholar
  100. Solter, D., and Knowles, B. B., 1978, Monoclonal antibody defining a stage-specific mouse embryonic antigen (SSEA-1), Proc. Natl. Acad. Sci. USA 75: 5565.PubMedCrossRefGoogle Scholar
  101. Sperry, R. W., 1963, Chemoaffinity in the orderly growth of mouse fiber patterns and connections, Proc. Natl. Acad. Sci. USA 50: 703–710.PubMedCrossRefGoogle Scholar
  102. Stamper, H. B., Jr., and Woodruff, J. J., 1976, Lymphocyte homing into lymph nodes: In vitro demonstration of the selective affinity of recirculating lymphocytes for high-endothelial venules, J. Exp. Med. 144: 828–833.PubMedCrossRefGoogle Scholar
  103. Stoolman, L. M., Tenforde, T. S., and Rosen, S. D., 1984, Phosphomannosyl receptors may participate in the adhesive interaction between lymphocytes and high endothelial venules, J. Cell Biol. 99: 1535 1540.Google Scholar
  104. Takeichi, M., 1986, Molecular basis for teratocarcinoma cell—cell adhesion, in: Developmental Biology, Vol. 2 ( L. M. Brounder, ed.), pp. 373–388, Plenum Press, New York.Google Scholar
  105. Takeichi, M., 1988, The cadherins: Cell—cell adhesion molecules controlling animal morphogenesis, Development 102: 639–655.PubMedGoogle Scholar
  106. Trisler, G. D., and Collins, F., 1987, Corresponding spatial gradients of TOP molecules in the developing retina and optic tectum, Science 237: 1208–1209.PubMedCrossRefGoogle Scholar
  107. Trisler, G. D., Schneider, M. D., and Nirenberg, M., 1981, A topographic gradient of molecules in retina can be used to identify neuron position, Proc. Natl. Acad. Sci. USA 78: 2145–2149.PubMedCrossRefGoogle Scholar
  108. Walter, J., Henke-Fahle, S., and Bonhoeffer, F., 1987a, Avoidance of posterior tectal membranes by temporal retina axons, Development 101:909–914.Google Scholar
  109. Walter, J., Kern-Veits, B., Huf, J., Stolze, B., and Bonhoeffer, F., 1987b, Recognition of position-specific properties of tectal cell membranes by retinal axons in vitro, Development 101: 685–696.PubMedGoogle Scholar
  110. Wassarman, P. M., 1987, Early events in mammalian fertilization, Annu. Rev. Cell Biol. 3:109–142. Yamada, T., 1985, Development of afferent fibre projections in rat spinal cord, Thesis, pp. 1–54, Tsukuba University.Google Scholar
  111. Yednock, T. A., Stoolman, L. M., and Rosen, S. D., 1987a, Phosphomannosyl-derivatized beads detect a receptor involved in lymphocyte homing, J. Cell Biol. 104: 713–723.PubMedCrossRefGoogle Scholar
  112. Yednock, T. A., Butcher, E. C., Stoolman, L. M., and Rosen, S. D., 1987b, Receptors involved in lymphocyte homing: Relationship between a carbohydrate-binding receptor and the MEL-14 antigen, J. Cell Biol. 104: 725–731.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1989

Authors and Affiliations

  • M. A. Hynes
    • 1
  • J. Dodd
    • 2
  • T. M. Jessell
    • 3
  1. 1.Howard Hughes Medical Institute, Center for Neurobiology and BehaviorColumbia University, College of Physicians and SurgeonsNew YorkUSA
  2. 2.Department of PhysiologyColumbia University, College of Physicians and SurgeonsNew YorkUSA
  3. 3.Howard Hughes Medical Institute, Center for Neurobiology and Behavior, and Department of Biochemistry and Molecular BiophysicsColumbia University, College of Physicians and SurgeonsNew YorkUSA

Personalised recommendations