Schwann cell heparan sulfate proteoglycans play a critical role in glial growth factor/neuregulin signaling

GLIA

Volumn 17, Issue 1, 1996, Pages 28-38

  Sudhalter, Judith ^a   Whitehouse, Laura ^b   Rusche, James R ^b   Marchionni, Mark A ^a   Mahanthappa, Nagesh K ^a,c  

^a CeNeS Pharmaceuticals plc   (United States)

^b ProsCure Inc   (United States)

^c Ontogeny Inc   (United States)

Author keywords

ARIA; c neu; erbB2; erbB3; erbB4; GGF; Heregulin; NDF; Rat

Indexed keywords

DNA; GLIA MATURATION FACTOR; GLYCOPROTEIN; NERVE GROWTH FACTOR; NERVE PROTEIN; NEU DIFFERENTIATION FACTOR; PROTEOGLYCAN;

ANIMAL; ARTICLE; CELL CULTURE; DOSE RESPONSE; DRUG EFFECT; HUMAN; PHYSIOLOGY; RAT; SCHWANN CELL; SIGNAL TRANSDUCTION;

ANIMALS; CELLS, CULTURED; DNA; DOSE-RESPONSE RELATIONSHIP, DRUG; GLIA MATURATION FACTOR; GLYCOPROTEINS; HUMANS; NERVE GROWTH FACTORS; NERVE TISSUE PROTEINS; NEUREGULINS; PROTEOGLYCANS; RATS; SCHWANN CELLS; SIGNAL TRANSDUCTION;

EID: 0030151356     PISSN: 08941491     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1098-1136(199605)17:1<28::AID-GLIA3>3.0.CO;2-3     Document Type: Article

References (59)

1. Adams, J.C. and Watt, F.M. (1993) Regulation of development and differentiation by the extracellular matrix. Development, 117: 1183-1198.
2. Brockes, J.P. (1987) Assay and isolation of glial growth factor from the bovine pituitary. Meth. Enzymol., 147:217-225.
3. Cardin, A.D. and Weintraub, H.J.R. (1989) Molecular modeling of protein-glycosaminoglycan interactions. Arteriosclerosis, 9:21-32.
4. Carey, D.J., Evans, D.M., Stahl, R C., Asundi, V.K., Conner, K.J., Garbes, P., and Cizmeci-Smith, G. (1992) Molecular cloning and characterization of N-syndecan, a novel transmembrane heparan sulfate proteoglycan. J. Cell Biol., 117:191-201.
5. Carey, D.J., Rafferty, C.M., and Todd, M.S. (1987) Effects of inhibition of proteoglycan synthesis on the differentiation of cultured rat Schwann cells. J. Cell Biol., 105:1013-1021.
6. Carey, D J., Stahl, R.C., Asundi, V.K., and Tucker, B. (1993) Processing and subcellular distribution of the Schwann cell lipid-anchored heparan sulfate proteoglycan and identification as glypican. Exp. Cell Res., 208:10-18.
7. Chen, M.S., Bermingham-McDonogh, O., Danehy, F.T., Nolan, C., Scherer, S.S., Lucas, J., Gwynne, D., and Marchionni, M.A. (1994) Expression of multiple neuregulin transcripts in postnatal rat brains. J. Comp. Neurol., 349:389-400.
8. Chernousov, M.A. and Carey, D.J. (1993) N-syndecan (syndecan 3) from neonatal rat brain binds basic fibroblast growth factor. J. Biol. Chem., 268:16810-16814.
9. Chu, G.C., Moscoso, L.M., Sliwkowski, M.X., and Merlie, J. P. (1995) Regulation of the acetycholine receptor ∈ subunit gene by recombinant ARIA: An in vitro model for transynaptic gene regulation. Neuron, 14:329-339.
10. Cohen, J.A., Yachnis, A.T., Arai, M., Davis, J.G., and Scherer, S.S. (1992) Expression of the neu proto-oncogene by Schwann cells during peripheral nerve development and Wallerian degeneration. J. Neurosci. Res., 31:622-634.
11. Coussens, L., Yang-Feng, T.L., Liao, Y.-C., Chen, E., Gray, A., McGrath, J., Seeburg, P.H., Liebermann, T.A., Schlessinger, J., Francke, U., Levinson, A., and Ullrich, A. (1985) Tyrosine kinase receptor with extensive homology to epidermal growth factor receptor shares chromosomal location with Neu oncogene. Science, 230:132-1139.
12. Falls, D.L., Rosen, K.M., Corfas, G., Lane, W.S , and Fischbach, G.D. (1993) ARIA, a protein that stimulates acetylcholine receptor synthesis, is a member of the neu ligand family. Cell, 72:801-815.
13. Gallagher, J.T. and Walker, A. (1985) Molecular distinctions between heparan sulfate and heparin. Biochem. J., 230:665-674.
14. Galligani, L., Hopwood, J., Sehwartz, N.B., and Dorfman, A. (1975) Stimulation of synthesis of free chondroitin sulfate chains β-D-xylosides in cultured cells. J. Biol. Chem., 250:5400-5406.
15. Gao, G. and Goldfarb, M. (1995) Heparin can activate a receptor tyrosine kinase. EMBO J., 14:2183-2190.
16. Goodearl, A.D.J., Davis, J.B., Mistry, K., Minghetti, L., Otsu, M., Waterfield, M.D., and Stroobant, P. (1993) Purification of multiple forms of glial growth factor. J. Biol. Chem., 268:18095-18102.
17. Ho, W.-H., Armanini, M.P., Nuijens, A., Phillips, H.S., and Osheroff, P.L. (1995) Sensory and motor neuron-derived factor. J. Biol. Chem., 270:14523-14532.
18. erbB2. Science,256: 1205-1210.
19. Jo, S.A., Zhu, C., Marchionni, M.A., and Burden, S.J. (1995) Neuregulins are concentrated at nerve-muscle synapses and activate ACh-receptor gene expression. Nature, 373:158-161.
20. Kan, M., Wang, F., Xu, J., Crabb, J.W., Hou, J., and McKeehan, W.K. (1993) An essential heparin-binding domain in the fibroblast growth factor receptor kinase. Science, 259:1918-1921.
21. Klagsburn, M. and Baird, A. (1991) A dual receptor system is required for basic fibroblast growth factor activity. Cell, 67:229-231.
22. Kraus, M.H., Fedi, P., Starks, V., Muraro, R., and Aaronson, S.A. (1993) Demonstration of ligand-dependent signaling by the erbB-3 tyrosine kinase and its constituitive activation in human breast tumor cells. Proc. Natl. Acad. Sci. U.S.A., 90:2900-2904.
23. Laemmli, U.K (1970) Cleavage of structural proteins during assembly of the head of the bacteriophage T4. Nature, 227:680-685.
24. LaRocca, R.V., Meer, J., Gilliat, R.W., Stein, C.A., Cassidy, J., Myers, C.E., and Dalakos, M.C. (1990) Suramin-induced polyneuropathy. Neurology, 40:954-959.
25. Lee, M.K. and Lander, A.D. (1991) Analysis of affinity and structural selectivity in the binding of proteins to glycosaminoglycans: development of a sensitive electrophorectic approach. Proc. Natl. Acad. Sci. U.S.A., 88:2768-2772.
26. Lemke, G.E. and Brockes, J.P. (1984) Identification and purification of glial growth factor. J. Neurosci., 4:75-83.
27. Levi, A.D.O., Bunge, R P., Lofgren, L.A., Meima, L., Hefti, F., Nikolics, K., and Slikowski, M.X. (1995) The influence of heregulins on human Schwann cell proliferation. J. Neurosci., 15:1329-1340.
28. Levitzki, A. and Gazit, A. (1995) Tyrosine kinase inhibition: An approach to drug development. Science, 267:1782-1788.
29. Litwack, E.D., Stipp, C.S., Kumbasar, A., and Lander, A.D. (1994) Neuronal expression of glypican, a cell surface glycosylphosphotidylinositol-anchored heparan sulfate proteoglycan, in the adult rat nervous system. J. Neurosci., 14:3713-3724.
30. Loeb, J.A. and Fischbach, G.D. (1995) ARIA can be released from extracellular matrix through cleavage of a heparin-binding domain. J. Cell Biol., 130:127-135.
31. Marchionni, M.A., Goodearl, A.D.J., Chen, M.S., Bermingham-McDonogh, O., Kirk, C., Hendricks, M., Danehy, F , Misumi, D., Sudhalter, J., Kobayashi, K., Wroblewski, D., Lynch, C., Baldassare, M., Hiles, I., Davis, J.B., Hsuan, J.J., Totty, N F., Otsu, M., McBurney, R.N., Waterfield, M.D., Stroobant, P., and Gwynne, D. (1993) Glial growth factors are alternatively spliced erbB2 ligands expressed in the nervous system. Nature, 362:312-318.
32. erbB2 are involved in axon-induced Schwann cell proliferation. Soc. Neurosci. Abstr., 20:707.
33. Moscatelli, D. (1987) High and low affinity binding sites for basic fibroblast growth factor on cultured cells: absence of a role for low affinity binding in the stimulation of plasminogen activator production by bovine capillary endothelial cells. J. Cell Physiol., 131: 123-130.
34. Moscatelli, D. and Quatro, N. (1989) Transformation of NIH 3T3 cells with basic fibroblast growth factor or the hst/K-fgf oncogene causes downregulation of the fibroblast growth factor receptor: reversal of morphological transformation and restoration of receptor number by suramin. J. Cell Biol., 109:2519-2527.
35. Mudge, A.W. (1993) New ligands for Neu? Curr. Biol., 3:361-364.
36. Nurcombe, V., Ford, M.D., Wildschut, J.A., and Bartlett, P.F. (1993) Developmental regulation of neural response to FGF-1 and FGF-2 by heparan sulfate proteoglycan. Science, 1993:103-106.
37. Ornitz, D.M., Yayon, A., Flanagan, J.G., Svahn, C.M., Levi, E., and Leder, P. (1992) Heparin is required for cell-free binding of bFGF to a soluble receptor and for mitogenesis in whole cells. Mol. Cell. Biol., 12:240-247.
38. Padhy, L.C., Shih, C., Cowing, D., Finkelstein, R., and Weinberg, R.A. (1982) Identification of phosphoprotein specifically induced by the transforming DNA of rat neuroblastomas. Cell, 23:865-872.
39. Peles, E., Bacus, S.S., Koski, R.A., Lu, H.S., Wen, D., Ogden, S.G., Ben-Levy, R., and Yarden, Y. (1992) Isolation of the Neu/Ne-2 stimulatory ligand: A 44 kD glycoprotein that induces differentiation of mammary tumor cells. Cell, 69:205-216.
40. Peles, E., Ben-Levy, R., Tzahar, E., Liu, N., Wen, D., and Yarden, Y. (1993) Cell-type specific interaction of Neu differentiation factor (NDF/heregulin) with Neu/Her-2 suggests complex ligand-receptor relationships. EMBO J., 12:961-971.
41. Peles, E. and Yarden, Y. (1993) Neu and its ligands: From an oncogene to neural factors. BioEssays, 15:815-824.
42. erbB4. Nature, 366:473-475.
43. Rapraeger, A.C., Krufka, A., and Olwin, B.B. (1991) Requirement of heparan sulfate for bFGF-mediated fibroblast growth and myoblast differentiation. Science, 252:1705-1708.
44. Ratner, N., Bunge, R.P., and Glaser, L. (1985) A neuronal cell surface heparan sulfate proteoglycan is required for dorsal root ganglion neuron stimulation of Schwann cell proliferation. J. Cell Biol., 101:744-754.
45. Ratner, N., Hong, D., Lieberman, M.A., Bunge, R.P., and Glaser, L. (1988) The neuronal cell-surface molecule mitogenic for Schwann cells is a heparin-binding protein. Proc. Natl. Acad Sci. U.S.A., 85:6992-6996.
46. Robinson, H.C., Brett, M.J., Tralaggan, P.J., Lowther, D.A , and Okayama, M. (1975) The effect of D-xylose, β-D-xylosides, and ß-D-galactosides on chondroitin sulphate biosynthesis in embryonic chicken cartilage. Biochem. J., 148:25-34.
47. Rutkowski, J.L., Kirk, C.J., Lerner, M.A., and Tennekoon, G.I. (1995) Purification and expression of human Schwann cells in vitro. Nature Med., 1:80-83.
48. Salzer, J.L., Bunge, R.P., and Glaser, L. (1980a) Studies of Schwann cell proliferation. III. Evidence for the surface localization of the neurite mitogen. J. Cell Biol., 84:767-778.
49. Salzer, J.L., Williams, A.K., Glaser, L., and Bunge, R.P. (1980b) Studies of Schwann cell proliferation. II. Characterization of the stimulation and specificity of the response to a neurite membrane fraction. J Cell. Biol., 84:753-766.
50. San Antonio, J.D., Slover, J., Lawler, J., Karnovsky, M. J., and Lander, A D. (1993) Specificity in the interactions of extracellular matrix proteins with subpopulations of the glycosaminoglycan heparin. Biochemistry, 32:4746-4755.
51. Spivak-Kroizman, T., Lemmon, M.A., Dikic, I., Ladbury, J.E., Pinchasi, D , Huang, J., Jaye, M., Crumley, G., Schlessinger, J., and Lax, I. (1994) Heparin-induced oligomerization of FGF molecules is responsible for FGF receptor dimerization, activation, and cell proliferation. Cell, 79:1015-1024.
52. Stipp, C.S., Litwack, E.D., and Lander, A.D. (1994) Cerebroglycan: An integral membrane heparan sulfate proteoglycan that is unique to the developing nervous system and expressed specifically during neuronal differentiation. J. Cell Biol., 124:149-160.
53. Sudhalter, J., Folkman, J., Svahn, C.M., Bergendal, K., and D'Amore, P.A. (1989) Importance of size, sulfation, and anticoagulant activity in the potentiation of acidic fibroblast growth factor by heparin. J. Biol. Chem., 264:6892-6897.
54. Towbin, H., Staehelin, T., and Gordon, J. (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. U.S.A., 76:4350-4354.
55. Wen, D., Peles, E., Cupples, R., Suggs, S.V., Bacus, S.S., Luo, Y., Trail, G., Hu, S., Silberger, S.M., Ben-Levy, R., Koski, R.A., Lu, H.S., and Yarden, Y (1992) Neu differentiation factor: a transmembrane glycoprotein containing an EGF domain and an immunoglobulin homology unit. Cell, 69:559-572.
56. Witt, D.P. and Lander, A.D. (1994) Differential binding of chemokines to glycosaminoglycan subpopulations. Curr. Biol., 4:394-400.
57. Yarden, Y. and Peles, E. (1991) Biochemical analysis of the ligand for the neu oncogenic receptor. Biochemistry, 30:3543-3550.
58. Yayon, A. and Klagsburn, M. (1990) Autocrine transformation by chimeric signal peptide-basic fibroblast growth factor: reversal by suramin. Proc. Natl. Acad. Sci. U.S.A., 87:5346-5350.
59. Yayon, A., Klagsburn, M., Esko, J.D., Leder, P., and Ornitz, D.M. (1991) Cell surface heparin-like molecules are required for binding of bFGF to its high affinity receptor. Cell, 64:841-848.