Skip to main content
SpringerLink
Log in

Expression and biological functions of sulfoglucuronyl glycolipids (SGGLs) in the nervous system—A review

  • Reviews
  • Published:
Neurochemical Research Aims and scope Submit manuscript

Abstract

Sulfoglucuronyl carbohydrate linked to neolactotetraose reacts with HNK-1 antibody. The HNK-1 carbohydrate epitope is found in two major glycolipids, several glycoproteins and in some proteoglycans of the nervous system. Most of the HNK-1 reactive glycoproteins so far identified are neural cell adhesion molecules and/or are involved in cell-cell interactions. HNK-1 carbohydrate is highly immunogenic. Several HNK-1-like antibodies, including IgM of some patients with plasma cell abnormalities and having peripheral neuropathy, have been described. This article summarizes published work mainly on sulfoglucuronyl glycolipids, SGGLs and covers: structural requirements of the carbohydrate epitope for binding to HNK-1 and human antibodies, expression of the lipids in various neural areas, stage and region specific developmental expression in CNS and PNS, immunocytochemical localization, loss of expression in Purkinje cell abnormality murine mutations, biosynthetic regulation of expression by a single enzyme N-acetylglucosaminyl transferase, identification of receptor-like carbohydrate binding neural proteins (lectins), and perceived role of the carbohydrate in physiological functions. The latter includes role in: pathogenesis of certain peripheral neuropathies, in migration of neural crest cells, as a ligand in cell-cell adhesion/interaction and as a promoter of neurite outgrowth for motor neurons. Multiple expression of HNK-1 carbohydrate in several molecules and in various neural cell types at specific stages of nervous system development has puzzled investigators as to its specific biological function, but this may also suggest its importance in multiple systems during cell differentiation and migration processes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Schachner, M. 1989. Families of neural adhesion molecules. Pages 56–172,in Back, G. and Harnett, S. (eds), Carbohydrate recognition in cellular function. Ciba Fdn. Symp. Vol. 145, John Wiley and Sons, Chichester, UK.

    Google Scholar 

  2. Jessell, T. M., Hynes, M. A., and Dodd, J. 1990. Carbohydrates and carbohydrate-binding proteins in the nervous system. Ann. Rev. Neurosci. 13:227–255.

    Google Scholar 

  3. Krog, L., and Bock, E. 1992. Glycosylation of neural cell adhesion molecules of the immunoglobulin superfamily. APMIS Suppl. 27 100:53–70.

    Google Scholar 

  4. Vogel, M., Kowalewski, H. J., Zimmermann, H., Janetzko, A., Margolis, R. J., and Wollny, H. E. 1991. Association of the HNK-1 epitope with 5′-nucleotidase fromTorpedo marmorata (electric ray) electric organ. Biochem. J. 278:199–202.

    Google Scholar 

  5. Mikol, D. D., Gulcher, J. R., and Stefansson, K. 1990. The oligodendrocyte-myelin glycoprotein belongs to a distinct family of proteins and contains the HNK-1 carbohydrate. J. Cell. Biol. 110:471–479.

    Google Scholar 

  6. Burger, D. D., Steck, A. J., Bernard, C. A., and DeRosbo, N. K. 1993. Human myelin/oligodendrocyte glycoproteins: A new member of the L2/HNK-1 family. J. Neurochem. 61:1822–1827.

    Google Scholar 

  7. Dieperink, M. E., O'Neill, A., Magnoni, G., Wollmann, R. L., Heinrikson, R.L., Sucher-Neely, H. A., and Stefansson, K. 1992. SAG: a Schwann cell membrane glycoprotein. J. Neurosci. 12:2177–2185.

    Google Scholar 

  8. Snipes, G. J., Suter, U., and Shooter, E. M. 1993. Human peripheral myelin protein-22 expresses the L2/HNK-1 carbohydrate adhesion epitope. J. Neurochem. 61:1961–1964.

    Google Scholar 

  9. Abo, T., and Balch, C. M. 1981. A differentiation antigen of human NK and K cells identified by a monoclonal antibody (HNK-1). J. Immunol. 127:1024–1029.

    Google Scholar 

  10. Margolis, R. K., Ripellino, J. A., Goossen, B., Steinbrich, R., and Margolis, R. U. 1987. Occurrence of HNK-1 epitope (3-sulfoglucuronic acid) in PC12 pheochromocytoma cells, chromaffin granule membrane and chondroitin sulfate proteoglycans. Biochem. Biophys. Res. Commun. 145:1142–1148.

    Google Scholar 

  11. Krueger, R. C., Hennig, A. K., and Schwartz, N. B. 1992. Two immunologically and developmentally distinct chondroitin sulfate proteoglycans in embryonic chick brain. J. Biol. Chem. 267:12149–12161.

    Google Scholar 

  12. Chou, D. K. H., Ilyas, A. A., Evans, J. E., and Jungalwala, F. B. 1985. Structure of a glycolipid reacting with monoclonal IgM in neuropathy and with HNK-1. Biochem. Biophys. Res. Commun. 128:383–388.

    Google Scholar 

  13. Chou, D. K. H., Ilyas, A. A., Evans, J. E., Costello, C., Quarles, R. H., and Jungalwala, F. B. 1986. Characterization of sulfated glucuronyl glycolipids in the nervous system reacting with HNK-S1 antibody and some IgM paraproteins in neuropathy. J. Biol. Chem. 261:11717–11725.

    Google Scholar 

  14. Ariga, T., Kohriyama, T., Freddo, L., Latov, N., Saito, M., Kon, K., Ando, S., Suzuki, M., Hemlin, M., Rinehart, K. L., Kusunoki, S., and Yu, R. K. 1987. Characterization of sulfated glucuronic acid containing glycolipids reacting with IgM-M proteins in patients with neuropathy. J. Biol. Chem. 262:848–853.

    Google Scholar 

  15. Kruse, J., Mailhammer, R., Wernecke, H., Faissner, A., Sommer, L., Goridis, C., and Schachner, M. 1984. Neural cell adhesion molecules and myelin associated glycoprotein share a common carbohydrate moiety recognized by monoclonal antibodies L2 and HNK-1. Nature (Lond.) 311:153–155.

    Google Scholar 

  16. Schwarting, G. A., Jungalwala, F. B., Chou, D. K. H., Boyer, A. M., and Yamamoto, M. 1987. Glucuronic acid and sulfate containing glycoconjugates are temporally and spatially regulated antigens in the developing mammalian central nervous system. Dev. Biol. 120:65–76.

    Google Scholar 

  17. Rougon, G., Hirsch, M. R., Hirn, M., Guenet, J. L., and Goridis, C. 1983. Monoclonal antibody to neural cell surface protein: identification of a glycoprotein family of restricted cellular localization. Neuroscience 10:511–520.

    Google Scholar 

  18. Kuchler, S., Zanetta, J.P., Bon, S., Zaepfel, M., Massoulie, J., and Vincendon, G. 1991. Expression and localization in the developing cerebellum of the carbohydrate epitopes revealed by ELEC-39, an IgM monoclonal antibody related to HNK-1. Neuroscience 41:551–562.

    Google Scholar 

  19. Merkouri, E., and Matsas, R. 1992. Monoclonal antibody BM89 recognizes a novel surface glycoprotein of the L2/HNK-1 family in the developing mammalian nervous system. Neuroscience 50:53–68.

    Google Scholar 

  20. Tucker, G. C., Aoyama, H., Lipinski, M., Thomas, T., and Thiery, J. P. 1984. Identical reactivity of monoclonal antibodies HNK-1 and NC-1: conservation in vertebrates on cells derived from the neural primordium and on some leukocytes. Cell Differ. 14:223–230.

    Google Scholar 

  21. Naegele, J. R., and Barnstable, C. J. 1991. A carbohydrate epitope defined by monoclonal antibody VC1.1 is found on N-CAM and other cell adhesion molecules. Brain Res. 559:118–129.

    Google Scholar 

  22. Braun, P. E., Frail, D. E., and Latov, N. 1982. Myelin-associated glycoprotein is the antigen for a monoclonal IgM in polyneuropathy. J. Neurochem. 39:1261–1265.

    Google Scholar 

  23. McGarry, R. C., Helfand, S. L., Quarles, R. H., and Roder, J. C. 1983. Recognition of a myelin-associated glycoprotein by the monoclonal antibody HNK-1. Nature (Lond) 306:366–378.

    Google Scholar 

  24. Ilyas, A. A., Quarles, R. H., Macintosh, T. D., Dobersen, M. J., Trapp, B. D., Dalakas, M. C., and Brady, R. O. 1984. IgM in a human neuropathy related to paraproteinemia binds to a carbohydrate determinant in the myelin associated glycoprotein and to a ganglioside. Proc. Natl. Acad. Sci. USA. 81:1225–1229.

    Google Scholar 

  25. Nakano, T., Ito, Y., and Ogawa, T. 1993. Synthesis of sulfated glucuronyl glycosphingolipids: carbohydrate epitopes of neural cell-adhesion molecules. Carbohyd. Res. 243:43–69.

    Google Scholar 

  26. Ilyas, A. A., Chou, D. K. H., Jungalwala, F. B., Costello, C., and Quarles, R. H. 1990. Variability in the structural requirements for binding of human monclonal anti-myelin-associated glycoprotein immunoglubulin M antibodies and HNK-1 to sphingogly-colipid antigens. J. Neurochem. 55:594–601.

    Google Scholar 

  27. Shashoua, V. E., Daniel, P. F., Moore, M. E., and Jungalwala, F. B. 1986. Demonstration of glururonic acid on brain glycoproteins which react with HNK-1 antibody. Biochem. Biophys. Res. Commun. 138:902–909.

    Google Scholar 

  28. Field, M. C., Wing, D. R., Dwek, R. A., Rademacher, T. W., Schmitz, B., Bollensen, E., and Schachner, M. 1992. Detection of multisulphated N-linked glycans in the L2/HNK-1 carbohydrate epitope expressing neural cell adhesion molecule P0. J. Neurochem. 58:993–1000.

    Google Scholar 

  29. Burger, D., Perruisseau, G., Simon, M., and Steck, A. J. 1992. Comparison of the N-linked oligosaccharide structures of the two major human myelin glycoproteins MAG and Po. Assessment and relative occurrence of oligosaccharide structures by serial lectin affinity chromatography of14C-glycopeptides. J. Neurochem. 58:845–853.

    Google Scholar 

  30. Kitamura, K., Tanaka, S., Sakamoto, Y., Shibuya, K., Yoshimura, K., Nomura, M., and Uyemura, K. 1993. Structural analyses of sulfated oligosaccharides from P0 glycoprotein in bovine peripheral nerve myelin. J. Neurochem. 61, (suppl.):S224.

    Google Scholar 

  31. Chou, D. K. H., Schwarting, G. A., Evans, J. E., and Jungalwala, F. B. 1987. Sulfoglucuronyl-neolacto series of glycolipids in peripheral nerves reacting with HNK-1 antibody. J. Neurochem. 49:865–873.

    Google Scholar 

  32. Shashoua, V. E., Jungalwala, F. B., Chou, D. K. H., and Moore, M. E. 1986. Sulfated glucuronyl glycoconjugates in ependymins of fish and human CSF. Trans. Am. Soc. Neurochem. 17:148.

    Google Scholar 

  33. Chou, D. K. H., Prasadarao, N., Koul, O., and Jungalwala, F. B. 1991. Developmental expression of HNK-1 reactive antigens in rat cerebral cortex and molecular heterogeneity of sulfoglucu-ronylneolactotetraosylceramide in CNS vs PNS. J. Neurochem. 57:852–859.

    Google Scholar 

  34. Prasadarao, N., Koul, O., Tobet, S. A., Chou, D. K. H., and Jungalwala, F. B. 1990. Developmental expression of HNK-1 reactive antigens in rat cerebellum and localization of sulfoglucuronyl glycolipids in molecular layer and deep cerebellar nuclei. J. Neurochem. 55:2024–2030.

    Google Scholar 

  35. Ariga, T., Kusunoki, S., Asano, K., Oshima, M., Asano, M., Mannen, T., and Yu, R. K. 1990. Localization of sulfated glucuronyl glycolipids in human dorsal root and sympathetic ganglia. Brain Res. 519:57–64.

    Google Scholar 

  36. Jungalwala, F. B., Chou, D. K. H., Suzuki, Y., and Maxwell, G. D. 1992. Temporal expression of HNK-1 reactive sulfoglucuronyl glycolipid in cell cultured quail trunk neural crest cells: Comparison with other developmentally regulated glycolipids. J. Neurochem. 58:1045–1051.

    Google Scholar 

  37. Miyatani, N., Kohriyama, T., Maeda, Y., and Yu, R. K. 1990. Sulfated glucuronyl paragloboside in rat brain microvessels. J. Neurochem. 55:577–582.

    Google Scholar 

  38. Chou, D. K. H. and Jungalwala, F. B. Unpublished Observations.

  39. Dennis, R. D., Antonicek, H., Wiegandt, H. and Schachner, M. 1988. Detection of L2/HNK-1 carbohydrate epitope on glycoproteins and acidic glycolipids of the insectCalliphora vicina. J. Neurochem. 51:1490–1496.

    Google Scholar 

  40. Breidbach, O., Dennis, R., Marx, J., Gorlach, C., Wiegandt, H., and Wegerhoff, R. 1992. Insect glial cells show differential expression of a glycolipid-derived, glucuronic acid-containing epitope throughout neurogenesis. Detection during post-embryogenesis and regeneration in the central nervous system ofTenebrio molitor L Neurosci. Lett. 147:5–8.

    Google Scholar 

  41. Willison, H. J., Ilyas, A. A., O'Shannessy, D. J., Pulley, M., Trapp, B. D., and Quarles, R. H. 1987. Myelin associated glycoprotein and related glycoconjugates in developing cat peripheral nerve: A correlative biochemical and morphometric study. J. Neurochem. 49:1853–1862.

    Google Scholar 

  42. Kohriyama, T., Kusunoki, S., Ariga, T., Yoshino, J. E., DeVries, G. H., Latov, N., and Yu, R. K. 1987. Subcellular localization of sulfated glucuronic-acid-containing lgycolipids reacting with anti-myelin associated glycoprotein antibody. J. Neurochem. 48:1516–1522.

    Google Scholar 

  43. Yamamoto, M., Marshall, P., Hemmendinger, L. M., Boyer, A. B., and Caviness, V. S. 1988. Distribution of glucuronic acid-and-sulfate-containing glycoproteins in the central nervous system of the adult mouse. Neurosci. Res. 5:273–298.

    Google Scholar 

  44. Wernecke, H., Linder, J., and Schachner, M. 1985. Cell type specificity and developmental expression of the L2/HNK-1 epitopes in mouse cerebellum. J. Neuroimmunol. 9:115–130.

    Google Scholar 

  45. Holley, J. A., and Yu, R. K. 1987. Localization of glycoconjugates recognized by the HNK-1 antibody in mouse and chick embryos during early neural development. Dev. Neurosci. 9:105–119.

    Google Scholar 

  46. Prasadarao, N., Tobet, S. A., and Jungalwala, F. B. 1990. Effect of different fixatives on immunocytochemical localization of HNK-1 reactive antigens in cerebeilum. A method for differentiating the localization of the same carbohydrate epitope on proteins versus lipids. J. Histochem. Cytochem. 38:1193–1200.

    Google Scholar 

  47. Nair, S. M., Prasadarao, N., Tobet, S. A., and Jungalwala, F. B. 1993. Rostrocaudal expression of antibody HNK-1 reactive glycolipids in mouse cerebellum: Relationship to developmental compartments and leaner mutation. J. Comp. Neurol. 332:282–292.

    Google Scholar 

  48. Altman, J., and Bayer, S. A. 1985. Embryonic development of the rat cerebellum. I. Delineation of the cerebellar primordium and early cell movements. J. Comp. Neurol. 237:1–26.

    Google Scholar 

  49. Schuller-Petrovic, S., Gebhart, W., Lassmann, H., Rumpold, H., and Kraft, D. 1983. A shared antigenic determinant between natural killer cells and nervous tissue. Nature (London). 306:179–181.

    Google Scholar 

  50. Nieke, J., and Schachner, M. 1985. Expression of neural cell adhesion molecule L1 and N-CAM and their common carbohydrate epitope L2/HNK-1 during development and after transection of the mouse sciatic nerve. Differentiation. 30:141–151.

    Google Scholar 

  51. Martini, R., Bollesen, E., and Schachner, M. 1988. Immunocytological localization of the major peripheral nervous system glycoprotein P0 and the L2/HNK-1 and L3 carbohydrate structures in developing and adult mouse sciatic nerve. Dev. Biol. 129:330–338.

    Google Scholar 

  52. Chou, D. K. H., and Jungalwala, F. B. 1988. Sulfoglucuronyl neolactoglycolipids in adult cerebellum: Specific absence in murine mutants with Purkinje cell abnormality. J. Neurochem. 50:1655–1658.

    Google Scholar 

  53. Chou, D. K. H., Flores, S., and Jungalwala, F. B. 1990. Loss of sulfoglucuronyl and other neolactoglycolipids in Purkinje cell abnormality murine mutants. J. Neurochem. 54:1589–1597.

    Google Scholar 

  54. Das, K., Basu, M., Basu, S., Chou, D. K. H., and Jungalwala, F. B. 1991 Biosynthesis in vitro of GlcAβ1-3nLcOse4Cer by a novel glucuronyltransferase (GlcAT-1) from embryonic chick brain. J. Biol. Chem. 266:5238–5243.

    Google Scholar 

  55. Das, K., Basu, M., Li, Z., Basu, S., and Jungalwala, F. B. 1990. Characterization of solubilized GlcAT-1 (UDP-GlcA:nLcOse4Cer β1-3glucuronyltransferase) activity from embryonic chicken brain and its inhibition by D-erythro-sphingosine. Ind. J. Biochem. Biophys. 27:396–401.

    Google Scholar 

  56. Chou, D. K. H., Flores, S., and Jungalwala, F. B. 1991. Expression and regulation of UDP-glucuron-ate: neolactotetraosylceramide glucuronyltransferase in the nervous system. J. Biol. Chem. 266:17941–17947.

    Google Scholar 

  57. Chou, D. K. H., and Jungalwala, F. B. 1993. Characterization and developmental expression of a novel sulfotransferase for the biosynthesis of sulfoglucuronyl glycolipids in the nervous system. J. Biol. Chem. 268:330–336.

    Google Scholar 

  58. Chou, D. K. H., and Jungalwala, F. B. 1994. Characterization and developmental expression of lactotriosylceramide: galactosyltransferase for the synthesis of neolactotetraosylceramide in the nervous system. J. Neurochem. 62:307–314.

    Google Scholar 

  59. Chou, D. K. H., and Jungalwala, F. B. 1993. N-acetylgluco-saminyltransferase regulates the expression of neolactoglycolipids including sulfoglucuronyl glycolipids in the developing nervous system. J. Biol. Chem. 268:21727–21733.

    Google Scholar 

  60. Jungalwala, F. B., and Chou, D. K. H. 1993. Expression and regulation of HNK-1 reactive sulfoglucuronyl glycolipids in the developing nervous system. J. Neurochem. 61 (suppl.):S159.

    Google Scholar 

  61. Andersen, B. B., Korbo, L., and Pakkenberg, B. 1992. A quantitative study of the human cerebellum with unbiased stereological techniques. J. Comp. Neurol. 326:549–560.

    Google Scholar 

  62. Korbo, L., Andersen, B. B., Ladefoged, O., and Moller, A. 1993. Total number of various cell types in rat cerebellar cortex estimated using an unbiased stereological method. Brain Res. 609:262–268.

    Google Scholar 

  63. Mohan, P. S., Chou, D. K. H., and Jungalwala, F. B. 1990. Sulfoglucuronyl glycolipids bind laminin. J. Neurochem. 54:2024–2031.

    Google Scholar 

  64. Roberts, D. D., Rao, C. N., Liotta, L. A., Gralnik, H. R., and Ginsburg, V. 1986. Comparison of the specificitiesos of laminin, thrombospondin and von Willebrand factor for binding to sulfated glycolipids. J. Biol. Chem. 261:6872–6877.

    Google Scholar 

  65. Mohan, P. S., Laitinen, J., Merenmies, J., Rauvala, H., and Jungalwala, F. B. 1992. Sulfoglycolipids bind to adhesive protein amphoterin (P30) in the nervous system. Biochem. Biophys. Res. Commun. 182:689–696.

    Google Scholar 

  66. Rauvala, H., and Pihlaskari, R. 1987. Isolation and some characteristics of an adhesive factor of brain that enhances neurite outgrowth in central neurons. J. Biol. Chem. 262:16625–16635.

    Google Scholar 

  67. Merenmies, J., Pihlaskari, R., Laitinen, J., Wartiovaar, J., and Rauvala, H. 1991. 30-kDa heparin binding protein of brain (Amphoterin) involved in neurite outgrowth. Amino acid sequence and localization in the filopodia of the advancing plasma membrane. J. Biol. Chem. 266:16722–16729.

    Google Scholar 

  68. Daston, M. M., and Ratner, N. 1991. Expression of P30, a protein with adhesive properties, in Schwann cells and neurons of developing and regenerating peripheral nerve. J. Cell Biol. 112:1229–1239.

    Google Scholar 

  69. parkkinen, J., Raulo, E., Merenmies, J., Nolo, R., Kajander, E. O., Baumann, M., and Rauvala, H. 1993. Amphoterin, the 30 kDa protein in a family of HMG1-type polypeptides. J. Biol. Chem. 268:19726–19738.

    Google Scholar 

  70. Rauvala, H. 1989. A 18-kDa heparin-binding protein of developing brain that is distinct from fibroblast growth factors. EMBO J. 8:2933–2941.

    Google Scholar 

  71. Merenmies, J., and Rauvala, H. 1990. Molecular cloning of 18-kDa growth associated protein of developing brain. J. Biol. Chem. 265:16721–16724.

    Google Scholar 

  72. Li, Y-S., Milner, P. G., Chauhan, A. K., Watson, M. A., Hoffman, R. M., Kodner, C. M., Milbrandt, J., and Duel, T. F. 1990. Cloning and expression of a developmentally regulated protein that induces mitogenic and neurite outgrowth activity. Science. 250:1690–1694.

    Google Scholar 

  73. Erbe, D. V., Watson, S. R., Presta, L. G., Wolizky, B. A., Foxall, C., Brandley, B. K., and Lasky, L. A. 1993. P-Selectin and E-Selectin use common sites for carbohydrate ligand recognition and cell adhesion. J. Cell Biol. 120:1227–1235.

    Google Scholar 

  74. Needham, L. K., and Schnaar, R. L. 1993. The HNK-1 reactive sulfoglucuronyl glycolipids are ligands for L-selectin and P-selectin but not E-selectin. Proc. Natl. Acad. Sci. USA. 90:1359–1363.

    Google Scholar 

  75. Needham, L. K., and Schnaar, R. L. 1993. Carbohydrate recognition in the peripheral nervous system: A calcium dependent membrane binding site for HNK-1 reactive glycolipids potentially involved in Schwann cell adhesion. J. Cell Biol. 121:397–408.

    Google Scholar 

  76. Quarles, R. H., Ilyas, A. A., and Willison, H. J. 1986. Antibodies to glycolipids in demyelinating disease of the human peripheral nervous system. Chem. Phys. Lipids. 42:235–248.

    Google Scholar 

  77. Khoriyama, T., Ariga, T., and Yu, R. K. 1988. Preparation and characterization of antibodies against a sulfated glucuronic acid-containing glycosphingolipid. J. Neurochem. 51:869–877.

    Google Scholar 

  78. Hayes, A. P., Latov, N., Takatsu, M., and Sherman, W. H. 1987. Experimental demyelination of nerve induced by serum of patients with neuropathy and an anti-MAG IgM M protein. Neurology 37:242–256.

    Google Scholar 

  79. Maeda, Y., Brosnan, C. F., Miyatani, N., and Yu, R. K. 1991. Preliminary studies on sensitization of Lewis rats with sulfated glucuronyl paragloboside. Brain Res. 541:257–264.

    Google Scholar 

  80. Maeda, Y., Bigbee, J. W., Maeda, R., Miyatani, N., Kalb, R. G., and Yu, R. K. 1991. Induction of demyelination by intraneural injection of antibodies against sulfoglucuronyl paragloboside. Expt. Neurol. 113:221–225.

    Google Scholar 

  81. Le Douarin, N. M. 1982. The neural crest. Cambridge University Press, Cambridge, U.K.

    Google Scholar 

  82. Hall, B. K., and Horstadius, S. 1988. The neural crest. Oxford University Press, London, U.K.

    Google Scholar 

  83. Rickmann, M., Fawcett, J. W., and Keynes, R. J. 1985. The migration of neural crest cells and the growth cones of motor axons through the rostral part of the chick somite. J. Embryol. Exp. Morphol. 90:437–455.

    Google Scholar 

  84. Bronner-Fraser, M. 1986. Analysis of the early stages of trunk neural crest migration in avian embryos using monoclonal antibody HNK-1. Dev. Biol. 115:44–55.

    Google Scholar 

  85. Loring, J. F., and Erickson, C. A. 1987. Neural crest migratory pathways in the trunk of the chick embryo. Dev. Biol. 121:220–236.

    Google Scholar 

  86. Luider, T. M., Peters-Vandersanden, M. J. H., Molenarar, J. C., Tibboel, D., Vanderkamp, A. W. M., and Meijers, C. 1992. Characterization of HNK-1 antigens during the formation of the avian enteric nervous system. Development 115:561–572.

    Google Scholar 

  87. Bronner-Fraser, M. 1987. Perturbation of cranial neural crest migration by the HNK-1 antibody. Dev. Biol. 123:321–331.

    Google Scholar 

  88. Maxwell, G. D., and Forbes, M. E. 1991. Spectrum of in vitro differentiation of quail trunk neural crest cells isolated by cell sorting using the HNK-1 antibody and analysis of the adrenergic development of HNK-1+ sorted subpopulations. J. Neurobiol. 22:276–286.

    Google Scholar 

  89. 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 

  90. Keilhauer, G., Faissner, A., and Schachner, M. 1985. Differential inhibition of neuron-neuron, neuron-astrocyte and astrocyte-astrocyte adhesion by L1, L2 and N-CAM antibodies. Nature (London) 316:728–730.

    Google Scholar 

  91. Martini, R., Xin, Y., Schnitz, B., and Schachner, M. 1992. The L2/HNK-1 carbohydrate epitope is involved in the preferential outgrowth of motor neurons on ventral roots and motor nerves. Europ. J. Neurosci. 4:628–639.

    Google Scholar 

  92. D'Urso, D., Brophy, P. J., Staugaltis, S. M., Gillespie, C. S., Frey, A. B., Stempak, J. G., and Colman, D. R. 1990. The protein zero of peripheral nerve myelin: biosynthesis, membrane insertion and evidence of homotypic interaction. Neuron 4:449–460.

    Google Scholar 

  93. Griffith, L. S., Schmitz, B., and Schachner, M. 1992. L2/HNK-1 carbohydrate and protein-protein interactions mediate the homophilic binding of the neural adhesion molecule P0. J. Neurosci. Res. 33:639–648.

    Google Scholar 

  94. Yazaki, T., Asou, H., Kitamura, K., Kotake, Y., and Uyemura, K. 1993. Functional domains of myelin P0 protein. J. Neurochem. 61 (suppl.):S224.

    Google Scholar 

  95. Oka, S., Terayama, K., Kawashima, C., and Kawasaki, T. 1992. A novel glucuronyltransferase in nervous system presumably associated with the biosynthesis of HNK-1 carbohydrate epitope on glycoproteins. J. Biol. Chem. 267:22711–22714.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biomedical Sciences, Eunice Kennedy Shriver Center, 200 Trapelo Road, 02254, Waltham, MA

    Firoze B. Jungalwala

  2. Department of Neurology, Harvard Medical School, 200 Trapelo Road, 02254, Boston, MA

    Firoze B. Jungalwala

Authors
  1. Firoze B. Jungalwala
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Special issue dedicated to Dr. Marjorie B. Lees.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Jungalwala, F.B. Expression and biological functions of sulfoglucuronyl glycolipids (SGGLs) in the nervous system—A review. Neurochem Res 19, 945–957 (1994). https://doi.org/10.1007/BF00968704

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00968704

Key Words

Search

Navigation