Polysialytransferase ST8Sia II (STX) polysialylates all of the major isoforms of NCAM and facilitates neurite outgrowth

Glycobiology

Volumn 11, Issue 3, 2001, Pages 231-239

  Franceschini, Isabelle ^a,c   Angata, Kiyohiko ^a   Ong, Edgar ^a   Hong, Allison ^a   Doherty, Patrick ^b   Fukuda, Minoru ^a  

^a BURNHAM INSTITUTE   (United States)

^b GUY S HOSPITAL   (United Kingdom)

^c INSTITUT PASTEUR   (France)

Author keywords

Neural cell adhesion molecule; Neurite cell outgrowth; Polysialic acid; Polysialyltransferase; ST8Sia II (STX)

Indexed keywords

GLYCOSYLPHOSPHATIDYLINOSITOL; ISOPROTEIN; NERVE CELL ADHESION MOLECULE; POLYPEPTIDE; POLYSIALIC ACID; SIALYLTRANSFERASE; CMP-N-ACETYLNEURAMINATE-POLY-ALPHA-2,8-SIALOSYL SIALYLTRANSFERASE; POLY ALPHA 2,8 SIALOSYL SIALYLTRANSFERASE; SIALIC ACID DERIVATIVE;

ANIMAL CELL; ARTICLE; CATALYSIS; CELL MEMBRANE; CELL STRAIN 3T3; CONTROLLED STUDY; FACILITATION; HYPOPHYSIS CELL; MODULATION; MOLECULAR SIZE; MOUSE; NERVE FIBER GROWTH; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; SIALYLATION; SIGNAL TRANSDUCTION; ANIMAL; GENETIC TRANSFECTION; GENETICS; HELA CELL; HUMAN; METABOLISM; NEURITE;

ANIMALIA;

3T3 CELLS; ANIMALS; HELA CELLS; HUMANS; MICE; NEURAL CELL ADHESION MOLECULES; NEURITES; PROTEIN ISOFORMS; SIALIC ACIDS; SIALYLTRANSFERASES; TRANSFECTION;

EID: 0034743945     PISSN: 09596658     EISSN: None     Source Type: Journal    
DOI: 10.1093/glycob/11.3.231     Document Type: Article

References (58)

1. Angata, K., Nakayama, J., Fredette, B., Chong, K., Ranscht, B., and Fukuda, M. (1997) Human STX polysialyltransferase forms the embryonic form of the neural cell adhesion molecule. Tissue-specific expression, neurite outgrowth, and chromosomal localization in comparison with another polysialyltransferase, PST. J. Biol. Chem., 272, 7182-7190.
2. Angata, K., Suzuki, M., and Fukuda, M. (1998) Differential and cooperative polysialylation of the neural cell adhesion molecule by two polysialyltransferases, PST and STX. J. Biol. Chem., 273, 28524-28532.
3. Beggs, H.E., Soriano, P., and Maness, P.F. (1994) NCAM-dependent neurite outgrowth is inhibited in neurons from Fyn-minus mice. J. Cell Biol., 127, 825-833.
4. Beggs, H.E., Baragona, S.C., Hemperly, J.J., and Maness, P.F. (1997) NCAM140 interacts with the focal adhesion kinase p125(fak) and the SRC-related tyrosine kinase p59(fyn). J. Biol. Chem., 272, 8310-8319.
5. Bottenstein, J.E. and Sato, G.H. (1979) Growth of a rat neuroblastoma cell line in serum-free supplemented medium. Proc. Natl Acad. Sci. USA, 76, 514-517.
6. Bourne, S.P., Patel, K., Walsh, F., Popham, C.J., Coakham, H.B., and Kemshead, J.T. (1991) A monoclonal antibody (ERIC-1), raised against retinoblastoma, that recognizes the neural cell adhesion molecule (NCAM) expressed on brain and tumours arising from the neuroectoderm. J. Neurooncol., 10, 111-119.
7. Chung, W.W., Lagenaur, C.F., Yan, Y.M., and Lund, J.S. (1991) Developmental expression of neural cell adhesion molecules in the mouse neocortex and olfactory bulb. J. Comp. Neurol., 314, 290-305.
8. Cremer, H., Lang, R., Christoph, A., Plomann, M., Vopper, G., Roes, J., Brown, R., Baldwin, S., Kraemer, P., Scheff, S., and others. (1994) Inactivation of the N-CAM gene in mice results in size reduction of the olfactory bulb and deficits in spatial learning. Nature, 367, 455-459.
9. Cremer, H., Chazal, G., Goridis, C., and Represa, A. (1997) NCAM is essential for axonal growth and fasciculation in the hippocampus. Mol. Cell. Neurosci., 8, 323-335.
10. Cunningham, B.A., Hoffman, S., Rutishauser, U., Hemperly, J.J., and Edelman, G.M. (1983) 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. USA, 80, 3116-3120.
11. Dahlin-Huppe, K., Berglund, E.O., Ranscht, B., and Stallcup, W.B. (1997) Mutational analysis of the L1 neuronal cell adhesion molecule identifies membrane-proximal amino acids of the cytoplasmic domain that are required for cytoskeletal anchorage. Mol. Cell. Neurosci., 9, 144-156.
12. Dickson, G., Gower, H.J., Barton, C.H., Prentice, H.M., Elsom, V.L., Moore, S.E., Cox, R.D., Quinn, C., Putt, W., and Walsh, F.S. (1987) Human muscle neural cell adhesion molecule (N-CAM): identification of a muscle-specific sequence in the extracellular domain. Cell, 50, 1119-1130.
13. Doherty, P., Cohen, J., and Walsh, F.S. (1990) Neurite outgrowth in response to transfected N-CAM changes during development and is modulated by polysialic acid. Neuron, 5, 209-219.
14. Doherty, P., Rowett, L.H., Moore, S.E., Mann, D.A., and Walsh, F.S. (1991) Neurite outgrowth in response to transfected N-CAM and N-cadherin reveals fundamental differences in neuronal responsiveness to CAMs. Neuron, 6, 247-258.
15. Doherty, P., Rimon, G., Mann, D.A., and Walsh, F.S. (1992) Alternative splicing of the cytoplasmic domain of neural cell adhesion molecule alters its ability to act as a substrate for neurite outgrowth. J. Neurochem., 58, 2338-2341.
16. Doherty, P., Williams, E., and Walsh, F.S. (1995) A soluble chimeric form of the L1 glycoprotein stimulates neurite outgrowth. Neuron, 14, 57-66.
17. Eckhardt, M., Muhlenhoff, M., Bethe, A., Koopman, J., Frosch, M., and Gerardy-Schahn, R. (1995) Molecular characterization of eukaryotic polysialyltransferase-1. Nature, 373, 715-718.
18. Eckhardt, M., Bukalo, O., Chazal, G., Wang, L., Goridis, C., Schachner, M., Gerardy-Schahn, R., Cremer, H., and Dityatev, A. (2000) Mice deficient in the polysialyltransferase ST8SiaIV/PST-1 allow discrimination of the roles of neural cell adhesion molecule protein and polysialic acid in neural development and synaptic plasticity. J. Neurosci., 20, 5234-5244.
19. Edelman, G.M. (1984) Modulation of cell adhesion during induction, histogenesis, and perinatal development of the nervous system. Annu. Rev. Neurosci., 7, 339-377.
20. Finne, J. (1982) Occurrence of unique polysialosyl carbohydrate units in glycoproteins of developing brain. J. Biol. Chem., 257, 11966-11970.
21. Fredette, B., Rutishauser, U., and Landmesser, L. (1993) Regulation and activity-dependence of N-cadherin, NCAM isoforms, and polysialic acid on chick myotubes during development. J. Cell Biol., 123, 1867-1888.
22. Gower, H.J., Barton, C.H., Elsom, V.L., Thompson, J., Moore, S.E., Dickson, G., and Walsh, F.S. (1988) Alternative splicing generates a secreted form of N-CAM in muscle and brain. Cell, 55, 955-964.
23. Groves, A.K., Entwistle, A., Jat, P.S., and Noble, M. (1993) The characterization of astrocyte cell lines that display properties of glial scar tissue. Dev. Biol., 159, 87-104.
24. He, H.T., Barbet, J., Chaix, J.C., and Goridis, C. (1986) Phosphatidylinositol is involved in the membrane attachment of NCAM-120, the smallest component of the neural cell adhesion molecule. EMBO J., 5, 2489-2494.
25. Hemperly, J.J., Edelman, G.M., and Cunningham, B.A. (1986) cDNA clones of the neural cell adhesion molecule (N-CAM) lacking a membrane-spanning region consistent with evidence for membrane attachment via a phosphatidylinositol intermediate. Proc. Natl Acad. Sci. USA, 83, 9822-9826.
26. Hildebrandt, H., Becker, C., Murau, M., Gerardy-Schahn, R., and Rahmann, H. (1998) Heterogeneous expression of the polysialyltransferases ST8Sia II and ST8/Sia IV during postnatal rat brain development. J. Neurochem., 71, 2339-2348.
27. Hoffman, S. and Edelman, G.M. (1983) Kinetics of homophilic binding by embryonic and adult forms of the neural cell adhesion molecule. Proc. Natl Acad. Sci. USA, 80, 5762-5766.
28. Kojima, N., Yoshida, Y., Kurosawa, N., Lee, Y.C., and Tsuji, S. (1995) Enzymatic activity of a developmentally regulated member of the sialyltransferase family (STX): evidence for alpha 2,8-sialyltransferase activity toward N-linked oligosaccharides. FEBS Lett., 360, 1-4.
29. Kojima, N., Tachida, Y., Yoshida, Y., and Tsuji, S. (1996) Characterization of mouse ST8Sia II (STX) as a neural cell adhesion molecule-specific polysialic acid synthase. Requirement of core alpha1,6-linked fucose and a polypeptide chain for polysialylation. J. Biol. Chem., 271, 19457-19463.
30. Kojima, N., Tachida, Y., and Tsuji, S. (1997) Two polysialic acid synthases, mouse ST8Sia II and IV, synthesize different degrees of polysialic acids on different substrate glycoproteins in mouse neuroblastoma Neuro2a cells. J. Biochem. (Tokyo), 122, 1265-1273.
31. Kurosawa, N., Yoshida, Y., Kojima, N., and Tsuji, S. (1997) Polysialic acid synthase (ST8Sia II/STX) mRNA expression in the developing mouse central nervous system. J. Neurochem., 69, 494-503.
32. Livingston, B.D. and Paulson, J.C. (1993) Polymerase chain reaction cloning of a developmentally regulated member of the sialyltransferase gene family. J. Biol. Chem., 268, 11504-11507.
33. Moore, S.E., Thompson, J., Kirkness, V., Dickson, J.G., and Walsh, F.S. (1987) Skeletal muscle neural cell adhesion molecule (N-CAM): changes in protein and mRNA species during myogenesis of muscle cell lines. J. Cell Biol., 105, 1377-1386.
34. Muller, D., Wang, C., Skibo, G., Toni, N., Cremer, H., Calaora, V., Rougon, G., and Kiss, J.Z. (1996) PSA-NCAM is required for activity-induced synaptic plasticity. Neuron, 17, 413-422.
35. Nakayama, J., Fukuda, M.N., Fredette, B., Ranscht, B., and Fukuda, M. (1995) Expression cloning of a human polysialyltransferase that forms the polysialylated neural cell adhesion molecule present in embryonic brain. Proc. Natl Acad. Sci. USA, 92, 7031-7035.
36. Nelson, R.W., Bates, P.A., and Rutishauser, U. (1995) Protein determinants for specific polysialylation of the neural cell adhesion molecule. J. Biol. Chem., 270, 17171-17179.
37. O'Connell, A.W., Fox, G.B., Barry, T., Murphy, K.J., Fichera, G., Foley, A.G., Kelly, J., and Regan, C.M. (1997) Spatial learning activates neural cell adhesion molecule polysialylation in a corticohippocampal pathway within the medial temporal lobe. J. Neurochem., 68, 2538-2546.
38. Oka, S., Bruses, J.L., Nelson, R.W., and Rutishauser, U. (1995) Properties and developmental regulation of polysialyltransferase activity in the chicken embryo brain. J. Biol. Chem., 270, 19357-19363.
39. Ong, E., Yeh, J.-C., Ding, Y., Hindsgaul, O., and Fukuda, M. (1998a) Expression cloning of a human sulfotransferase that directs the synthesis of the HNK-1 glycan on the neural cell adhesion molecule and glycolipids. J. Biol. Chem., 273, 5190-5195.
40. Ong, E., Nakayama, J., Angata, K., Reyes, L., Katsuyama, T., Arai, Y., and Fukuda, M. (1998b) Developmental regulation of polysialic acid synthesis in mouse directed by two polysialyltransferases, PST and STX. Glycobiology, 8, 415-424.
41. Phillips, G.R., Krushel, L.A., and Crossin, K.L. (1997) Developmental expression of two rat sialyltransferases that modify the neural cell adhesion molecule, N-CAM. Brain Res. Dev. Brain Res., 102, 143-155.
42. Pollerberg, G.E., Schachner, M., and Davoust, J. (1986) Differentiation state-dependent surface mobilities of two forms of the neural cell adhesion molecule. Nature, 324, 462-465.
43. Pollerberg, G.E., Burridge, K., Krebs, K.E., Goodman, S.R., and Schachner, M. (1987) The 180-kD component of the neural cell adhesion molecule N-CAM is involved in a cell-cell contacts and cytoskeleton-membrane interactions. Cell Tissue Res., 250, 227-236.
44. Rutishauser, U. and Landmesser, L. (1991) Polysialic acid on the surface of axons regulates patterns of normal and activity-dependent innervation. Trends Neurosci., 14, 528-532.
45. Sadoul, R., Him, M., Deagostini-Bazin, H., Rougon, G., and Goridis, C. (1983) Adult and embryonic mouse neural cell adhesion molecules have different binding properties. Nature, 304. 347-349.
46. Saffell, J.L., Williams, E.J., Mason, I.J., Walsh, F.S., and Doherty, P. (1997) Expression of a dominant negative FGF receptor inhibits axonal growth and FGF receptor phosphorylation stimulated by CAMs. Neuron, 18, 231-242.
47. Schachner, M. and Martini, R. (1995) Glycans and the modulation of neural-recognition molecule function. Trends Neurosci., 18, 183-191.
48. Scheidegger, E.P., Sternberg, L.R., Roth, J., and Lowe, J.B. (1995) A human STX cDNA confers polysialic acid expression in mammalian cells. J. Biol. Chem., 270, 22685-22688.
49. Seki, T. and Arai, Y. (1991) Expression of highly polysialylated NCAM in the neocortex and piriform cortex of the developing and the adult rat. Anat. Embryol., 184, 395-401.
50. Seki, T. and Rutishauser, U. (1998) Removal of polysialic acid-neural cell adhesion molecule induces aberrant mossy fiber innervation and ectopic synaptogenesis in the hippocampus. J. Neurosci., 18, 3757-3766.
51. Simmons, D.L. (1993) Cloning cell surface molecules by transient expression in mammalian cells. In Hartly, D. (ed.), Cellular Interactions in Development. Oxford University Press, Oxford, UK, pp. 93-127.
52. Small, S.J. and Akeson, R. (1990) Expression of the unique NCAM VASE exon is independently regulated in distinct tissues during development. J. Cell Biol., 111, 2089-2096.
53. Sunshine, J., Balak, K., Rutishauser, U., and Jacobson, M. (1987) Changes in neural cell adhesion molecule (NCAM) structure during vertebrate neural development. Proc. Natl Acad. Sci. USA. 84, 5986-5990.
54. Tomasiewicz, H., Ono, K., Yee, D., Thompson, C., Goridis, C., Rutishauser, U., and Magnuson, T. (1993) Genetic deletion of a neural cell adhesion molecule variant (N-CAM-180) produces distinct defects in the central nervous system. Neuron, 11, 1163-1174.
55. Tsuboi, S. and Fukuda, M. (1997) Branched O-linked oligosaccharides ectopically expressed in transgenic mice reduce primary T-cell immune responses. EMBO J., 16, 6364-6373.
56. Walsh, F.S. and Doherty, P. (1996) Cell adhesion molecules and neuronal regeneration. Curr. Opin. Cell Biol., 8, 707-713.
57. Yoshida, Y., Kojima, N., and Tsuji, S. (1995) Molecular cloning and characterization of a third type of N-glycan alpha 2,8-sialyltransferase from mouse lung. J. Biochem. (Tokyo), 118, 658-664.
58. Zhang, H., Miller, R.H., and Rutishauser, U. (1992) Polysialic acid is required for optimal growth of axons on a neuronal substrate. J. Neurosci., 12, 3107-3114.