HB-GAM (heparin-binding growth-associated molecule) and heparin-type glycans in the development and plasticity of neuron-target contacts

Progress in Neurobiology

Volumn 52, Issue 2, 1997, Pages 127-144

  Rauvala, Heikki ^a   Peng, H Benjamin ^b  

^a UNIVERSITY OF HELSINKI   (Finland)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCAN DERIVATIVE; HEPARIN DERIVATIVE; PLEIOTROPHIN; SYNDECAN;

EXTRACELLULAR MATRIX; GROWTH CONE; HIPPOCAMPUS; HUMAN; NERVE CELL DIFFERENTIATION; NERVE CELL PLASTICITY; NERVE FIBER GROWTH; NERVE PROJECTION; NONHUMAN; PRIORITY JOURNAL; REVIEW;

EID: 0030905752     PISSN: 03010082     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0301-0082(97)00007-5     Document Type: Article

References (136)

1. Anderson, M. J. (1986) Nerve-induced remodeling of muscle basal lamina during synaptogenesis. J. Cell Biol. 102, 863-877.
2. Anderson, M. J. and Cohen, M. W. (1977) Nerve-induced and spontaneous redistribution of acetylcholine receptors on cultured muscle cells. J. Physiol. (Lond.) 268, 757-773.
3. Anderson, M. J. and Fambrough, D. M. (1983) Aggregates of acetyicholine receptors are associated with plaques of a basal lamina heparan sulfate proteoglycan on the surface of skeletal muscle fibers. J. Cell Biol. 97, 1396-1411.
4. Anderson, M. J., Klier, F. G. and Tanguay, K. E. (1984) Acetylcholine receptor aggregation parallels the deposition of a basal lamina proteoglycan. J. Cell Biol. 99, 1769-1784.
5. Asundi, V. K. and Carey, D. J. (1995) Self-association of N-syndecan (syndecan-3) core protein is mediated by a novel structural motif in the transmembrane domain and ectodomain flanking region. J. biol. Chem. 270, 26404-26410.
6. Aviezer, D., Hecht, D., Safran, M., Eisinger, M., David, G. and Yayon, A. (1994) Perlecan, basal lamina proteoglycan, promotes basic fibroblast growth factor receptor-binding, mitogenesis, and angiogenesis. Cell 79, 1005-1013.
7. Baker, L. P., Chen, Q. and Peng, H. B. (1992) Induction of acetylcholine receptor clustering by native polystyrene beads: implication of an endogenous muscle-derived signalling system. J. Cell Sci. 102, 543-555.
8. Bayne, E. K., Anderson, M. J. and Fambrough, D. M. (1984) Extracellular matrix organization in developing muscle: correlation with acetylcholine receptor aggregates. J. Cell Biol. 99, 1486-1501.
9. Bayer, S. A. and Altman, J. (1991) Neocortical Development. Raven Press: New York.
10. Bixby, J. L. and Harris, W. A. (1991) Molecular mechanisms of axon growth and guidance. Ann. Rev. Cell Biol. 7, 117-159.
11. Bloch, B., Normand, E., Kovesdi, I. and Böhlen, P. (1992) Expression of the HBNF (heparin-binding neurite-promoting factor) gene in the brain of fetal, neonatal and adult rat: an in situ hybridization study. Dev. Brain Res. 70, 267-278.
12. Bowe, M. A., Deyst, K. A., Leszyk, J. D. and Fallon, J. R. (1994) Identification and purification of an agrin receptor from Torpedo postsynaptic membranes: a heteromeric complex related to the dystroglycans. Neuron 12, 1173-1180.
13. Bowe, M. A. and Fallon, J. R. (1995) The role of agrin in synapse formation. Ann. Rev. Neurosci. 18, 443-462.
14. Campanelli, J. T., Roberds, S. L., Campbell, K. P. and Scheller, R. H. (1994) A role for dystrophin-associated glycoproteins and utrophin in agrin-induced AChR clustering. Cell 77, 663-674.
15. 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.
16. Daggett, D. F., Stone, D., Peng, H. B. and Nikolics, K. (1996a) Full-length agrin isoform activities and binding site distributions on cultured Xenopus muscle cells. Mol. Cell. Neurosci. 7, 75-88.
17. Daggett, D. F., Cohen, M. W., Stone, D., Nikolics, K., Rauvala, H. and Peng, H. B. (1996b) The role of an agrin-growth factor interaction in ACh receptor clustering. Mol. Cell. Neurosci. 8, 272-285.
18. Dai, Z. and Peng, H. B. (1996) From neurite to nerve terminal: induction of presynaptic differentiation by target-derived signals. Sem. Neurosci. 8, 97-106.
19. DeChiara, T. M., Bowen, D. C., Valenzuela, D. M., Simmons, M. V., Poueymirou, W. T., Thomas, S., Kinetz, E., Compton, D. L., Rojas, E., Park, J. S., Smith, C., DiStefano, P. S., Glass, D. J., Burden, S. J. and Yancopoulos, G. D. (1996) The receptor tyrosine kinase MuSK is required for neuromuscular junction formation in vivo. Cell 85, 501-512.
20. Desai, C. J., Gindhart, J. G. Jr, Goldstein, L. S. B. and Zinn, K. (1996) Receptor tyrosine phosphatases are required for motor axon guidance in the Drosophila embryo. Cell 84, 599-609.
21. Ervasti, J. M. and Campbell, K. P. (1993) A role for the dystrophin-glycoprotein complex as a transmembrane linker between laminin and actin. J. Cell Biol. 122, 809-823.
22. Ferns, M., Hoch, W., Campanelli, J. T., Rupp, F., Hall, Z. W. and Scheller, R. H. (1992) RNA splicing regulates agrin-mediated acetylcholine receptor clustering activity on cultured myotubes. Neuron 8, 1079-1086.
23. Ferns, M. J., Campanelli, J. T., Hoch, W., Scheller, R. H. and Hall, Z. (1993) The ability of agrin to cluster AChRs depends on alternative splicing and on cell surface proteoglycans. Neuron 11, 491-502.
24. Flaumenhaft, R., Moscatelli, D. and Rifkin, D. B. (1990) Heparin and heparan sulfate increase the radius of diffusion and action of basic fibroblast growth factor. J. Cell Biol. 111, 1651-1659.
25. Ganju, P., Walls, E., Brennan, J. and Reith, A. D. (1995) Cloning and developmental expression of Nsk2, a novel receptor tyrosine kinase implicated in skeletal myogenesis. Oncogene 11, 281-290.
26. Gao, G. and Goldfarb, M. (1995) Heparin can activate a receptor tyrosine kinase. EMBO J. 14, 2183-2190.
27. Gautam, M., Noakes, P. G., Moscoso, L., Rupp, F., Scheller, R. H., Merlie, J. P. and Sanes, J. R. (1996) Defective neuromuscular synaptogenesis in agrin-deficient mutant mice. Cell 85, 525-535.
28. Gee, S. H., Montanaro, F., Lindenbaum, M. H. and Carbonetto, S. (1994) Dystroglycan-a, a dystrophin-associated glycoprotein, is a functional agrin receptor. Cell 77, 675-686.
29. Gesemann, M., Cavalli, V., Denzer, A. J., Brancaccio, A., Schumacher, B. and Ruegg, M. A. (1996) Alternative splicing of agrin alters its binding to heparin, dystroglycan, and the putative agrin receptor. Neuron 16, 755-767.
30. Gesemann, M., Denzer, A. J. and Ruegg, M. A. (1995) Acetylcholine receptor-aggregating activity of agrin isoforms and mapping of the active site. J. Cell Biol. 128, 625-636.
31. Glass, D. J., Bowen, D. C., Stitt, T. N., Radziejewski, C., Bruno, J., Ryan, T. E., Gies, D. R., Shah, S., Mattsson, K., Burden, S. J., DiStefano, P. S., Valenzuela, D. M., DeChiara, T. M. and Yancopoulos, G. D. (1996) Agrin acts via a MuSK receptor complex. Cell 85, 513-523.
32. Hall, Z. W. and Sanes, J. R. (1993) Synaptic structure and development: the neuromuscular junction. Neuron 10, 99-121.
33. Hampton, B. S., Marshak, D. R. and Burgess, W. H. (1992) Structural and functional characterization of full-length heparin-binding growth-associated molecule. Mol. Biol. Cell 3, 85-93.
34. Hirano, Y. and Kidokoro, Y. (1989) Heparin and heparan sulfate partially inhibit induction of acetylcholine receptor accumulation by nerve in Xenopus culture. J. Neurosci. 9, 1555-1561.
35. Hoch, W., Ferns, M., Campanelli, J. T., Hall, Z. W. and Scheller, R. H. (1993) Developmental regulation of highly active alternatively spliced forms of agrin. Neuron 11, 479-490.
36. Hynes, R. O. and Lander, A. D. (1992) Contact and adhesive specificities in the associations, migrations, and targeting of cells and axons. Cell 68, 303-322.
37. Iozzo, R. V. (1994) Perlecan: a gem of a proteoglycan. Matrix Biol. 14, 203-208.
38. Iozzo, R. V. and Murdoch, A. D. (1996) Proteoglycans of the extracellular environment: clues from the gene and protein side offer novel perspectives in molecular diversity and function. FASEB J. 10, 598-614.
39. Jacobson, M. (1991) Developmental Neurobiology. Plenum Press: New York.
40. Kadomatsu, K., Tomomura, M. and Muramatsu, T. (1988) cDNA cloning and sequencing of a new gene intensely expressed in differentiation stages of embryonal carcinoma cells and in mid-gestation period of mouse embryogenesis. Biochem. Biophys. Res. Commun. 151, 1312-1318.
41. Kinnunen, T., Raulo, E., Nolo, R., Maccarana, M., Lindahl, U. and Rauvala, H. (1996a) Neunte outgrowth in brain neurons induced by heparin-binding growth-associated molecule (HB-GAM) depends on the specific interaction of HB-GAM with heparan sulfate at the cell surface. J. biol. Chem. 271, 2243-2248.
42. Kinnunen, A., Niemi, M., Nolo, R., Kinnunen, T., Kaksonen, M. and Rauvala, H. (1996b) HB-GAM (heparin-binding growth-associated molecule) and N-syndecan play a role in the formation of thalomocortical connections?. Soc. Neurosci. Abstr. 22, 386.11.
43. Kjellén, L. and Lindahl, U. (1991) Proteoglycans: structures and interactions. Annu. Rev. Biochem. 60, 443-475.
44. Klagsbrun, M. and Baird, A. (1991) A dual receptor system is required for basic fibroblast growth factor activity. Cell 67, 229-231.
45. Ko, P. K., Anderson, M. J. and Cohen, M. W. (1977) Denervated skeletal muscle fibers develop discrete patches of high acetylcholine receptor density. Science 196, 540-542.
46. Kretschmer, P. J., Fairhurst, J, L., Decker, M. M., Chan, C. P., Gluzman, Y., Böhlen, P. and Kovesdi, I. (1991) Cloning, characterization and developmental regulation of two members of a novel human gene family of neurite outgrowth-promoting proteins. Growth Fact. 5, 99-114.
47. Krueger, N. X., Vactor, D. V., Wan, H. I., Gelbart, W. M., Goodman, C. S. and Saito, H. (1996) The transmembrane tyrosine phosphatase DLAR controls motor axon guidance in Drosophila. Cell 84, 611-622.
48. Kuo, M.-D., Oda, Y., Huang, J. S. and Huang, S. S. (1990) Amino acid sequence and characterization of a heparin-binding neurite-promoting factor (p18) from bovine brain. J. biol. Chem. 265, 18749-18752.
49. Kuromi, H. and Kidokoro, Y. (1984) Nerve disperses preexisting acetylcholine receptor clusters prior to induction of receptor. Dev. Biol. 103, 53-61.
50. Kuwada, J. Y. (1986) Cell recognition by neuronal growth cones in a simple vertebrate embryo. Science 233, 740-746.
51. Lander, A. D. (1989) Understanding the molecules of neural cell contacts: emerging patterns of structure and function. Trends Neurosci. 12, 189-195.
52. Lauri, S. E., Taira, T., Kaila, K. and Rauvala, H. (1996a) Activity-induced enhancement of HB-GAM expression in hippocampal slices. NeuroReport 7, 1670-1674.
53. Lauri, S. E., Taira, T., Kaila, K. and Rauvala, H. (1996b) Activity-induced enhancement of HB-GAM expression in hippocampal slices: implications for long-term potentiation?. Soc. Neurosci. Abstr. 22, 600.15.
54. Lebakken, C. S. and Rapraeger, A. (1996) Syndecan-1 mediates cell spreading in transfected human lymphoblastoid (Raji) cells. J. Cell Biol. 132, 1209-1221.
55. Letourneau, P. C., Condic, M. L. and Snow, D. M. (1994) Interactions of developing neurons with the extracellular matrix. J. Neurosci. 14, 915-928.
56. Li, Y.-S., Milner, P. G., Chauhan, A. K., Watson, M. A., Hoffman, R. M., Kodner, C. M., Milbrandt, J. and Deuel, T. F. (1990) Cloning and expression of a developmentally regulated protein that induces mitogenic and neunte outgrowth activity. Science 250, 1690-1694.
57. Lieth, E., Cardasis, C. A. and Fallon, J. R. (1992) Muscle-derived agrin in cultured myotubes: expression in the basal lamina and at induced acetylcholine receptor clusters. Dev. Biol. 149, 41-54.
58. Lieth, E. and Fallon, J. R. (1993) Muscle agrin: neural regulation and localization at nerve-induced acetylcholine receptor clusters. J. Neurosci. 13, 2509-2514.
59. Lindahl, U., Lidholt, K., Spillmann, D. and Kjellén, L. (1994) More to "heparin" than anticoagulation. Thromb. Res. 75, 1-32.
60. Lyon, M., Deakin, J. A., Mizuno, K., Nakamura, T. and Gallagher, J. T. (1994) Interaction of hepatocyte growth factor with heparan sulfate. Elucidation of the major heparan sulfate structural determinants. J. biol. Chem. 269, 11216-11223.
61. Ma, E., Morgan, R. and Godfrey, E. W. (1994) Distribution of agrin mRNAs in the chick embryo nervous system. J. Neurosci. 14, 2943-2952.
62. Maccarana, M., Casu, B. and Lindahl, U. (1993) Minimal sequence in heparin/heparan sulfate required for binding of basic fibroblast growth factor. J. biol. Chem. 268, 23893-23905.
63. Maeda, N., Nishiwaki, T., Shintani, T., Hamanaka, H. and Noda, M. (1996) 6B4 proteoglycan/phosphacan, an extracellular variant of receptor-like protein-tyrosine phosphatase zeta/ RPTBβ, binds pleiotrophin heparin-binding growth-associated molecule (HB-GAM). J. biol. Chem. 271, 21446-21452.
64. Mahmood, R., Bresnick, J., Hornbruch, A., Mahony, K., Morton, N., Colquhoun, K., Martin, P., Lumsden, A., Dickson, C. and Mason, I. (1995) A role for FGF-8 in the initiation and maintenance of vertebrate limb bud outgrowth. Curr. Biol. 5, 797-806.
65. Marin-Padilla, M. (1978) Dual origin of the mammalian neocortex and evolution of the cortical plate. Anat. Embryol. 152, 109-126.
66. Matsubara, S., Tomomura, M., Kadomatsu, K. and Muramatsu, T. J. (1990) Structure of a retinoic acid-responsive gene, MK, which is transiently activated during the differentiation of embryonal carcinoma cells and the mid-gestation period of mouse embryogenesis. J. biol. Chem. 265, 9441-9443.
67. Matsumoto, K., Wanaka, A., Takatsuji, K., Muramatsu, H., Muramatsu, T. and Tohyama, M. (1994) A novel family of heparin-binding growth factors, pleiotrophin and midkine, is expressed in the developing rat cerebral cortex. Dev. Brain Res. 79, 229-241.
68. Matsumura, K. and Campbell, K. P. (1994) Dystrophin-glycoprotein complex: its role in the molecular pathogenesis of muscular dystrophies. Muscle Nerve 17, 2-15.
69. McGuire, P. G. and Seeds, N. W. (1990) Degradation of underlying extracellular matrix by sensory neurons during neurite outgrowth. Neuron 4, 633-642.
70. Maurel, P., Rauch, U., Flad, M., Margolis, R. K. and Margolis, R. U. (1994) Phosphacan, a chondroitin sulfate proteoglycan of brain that interacts with neurons and neural cell-adhesion molecules, is an extracellular variant of receptor-type tyrosine phosphatase. Proc. natn. Acad. Sci. U.S.A. 91, 2512-2516.
71. McMahan, U. J., Horton, S. E., Werle, M. J., Honig, L. S., Kroger, S., Ruegg, M. A. and Escher, G. (1992) Agrin isoforms and their role in synaptogenesis. Curr. Opin. Cell Biol. 4, 869-874.
72. Merenmies, J. (1992) Cell density-dependent expression of heparin-binding growth-associated molecule (HB-GAM, p18) and its downregulation by fibroblast growth factors. FEBS Lett. 307, 297-300.
73. Merenmies, J. and Rauvala, H. (1990) Molecular cloning of the 18 kDa growth-associated protein of developing brain. J. biol. Chem. 265, 16721-16724.
74. Milev, P., Friedlander, D. R., Sakurai, T., Karthikeyan, L., Flad, M., Margolis, R. K., Grumet, M. and Margolis, R. U. (1994) Interactions of the chondroitin sulfate proteoglycan phosphacan, the extracellular domain of a receptor-type tyrosine phosphatase, with neurons, glia, and neural cell adhesion molecules. J. Cell Biol. 127, 1703-1715.
75. Milner, P. G., Li, Y.-S., Hoffman, R. M., Kodner, C. M., Siegel, N. R. and Deuel, T. F. (1989) A novel 17 kDa heparin-binding growth factor (HBGF-8) in bovine uterus: purification and N-terminal amino acid sequence. Biochem. Biophys. Res. Commun. 165, 1096-1103.
76. Mitsiadis, T. A., Salmivirta, M., Muramatsu, T., Muramatsu, H., Rauvala, H., Lehtonen, E., Jalkanen, M. and Thesleff, I. (1995) Expression of the heparin-binding cytokines midkine (MK) and HB-GAM (pleiotrophin) is associated with epithelial-mesenchymal interactions during fetal development and organogenesis. Development 121, 37-51.
77. Molnár, Z. and Blakemore, C. (1995) How do thalamic axons find their way to the cortex?. Trends Neurosci. 18, 389-397.
78. Moody-Corbett, F. and Cohen, M. W. (1982) Influence of nerve on the formation and survival of acetylcholine receptor and cholinesterase patches on embryonic Xenopus muscle cells in culture. J. Neurosci. 2, 633-646.
79. Muramatsu, H. and Muramatsu, T. (1991) Purification of recombinant midkine and examination of its biological activities: functional comparison of new heparin binding growth factors. Biochem. Biophys. Res. Commun. 177, 652-658.
80. Murdoch, A. D., Liu, B., Schwarting, R., Tuan, R. S. and Iozzo, R. V. (1994) Widespread expression of perlecan proteoglycan in basement membranes and extracellular matrices of human tissues as detected by a novel monoclonal antibody against domain III and by in situ hybridization. J. Histochem. Cytochem. 42, 239-249.
81. Niswander, L. and Martin, G. R. (1993) FGF-4 and BMP-2 have opposite effects on limb growth. Nature 361, 68-71.
82. Niswander, L., Tickle, C., Vogel, A., Booth, I. and Martin, G. R. (1994) FGF-4 replaces the apical ectodermal ridge and directs outgrowth and patterning of the limb. Cell 75, 579-587.
83. Nolo, R., Kaksonen, M., Raulo, E. and Rauvala, H. (1995) Co-expression of heparin-binding growth-associated molecule (HB-GAM) and N-syndecan (syndecan-3) in developing rat brain. Neurosci. Lett. 191, 39-42.
84. Nolo, R., Kaksonen, M. and Rauvala, H. (1996) Developmentally regulated neurite outgrowth response from dorsal root ganglia neurons to heparin-binding growth-associated molecule (HB-GAM) and the expression of HB-GAM in the targets of the developing dorsal root ganglia neurites. Eur. J. Neurosci. 8, 1658-1665.
85. Noonan, D. M., Fulle, A., Valente, P., Cai, S., Horigan, E., Sasaki, M., Yamada, Y. and Hassell, J. R. (1991) The complete sequence of perlecan, a basement membrane heparan sulfate proteoglycan, reveals extensive similarity with laminin A chain, low density lipoprotein receptor, and the neural cell adhesion molecule. J. biol. Chem. 266, 22939-22947.
86. Nurcombe, V., Fraser, N., Herlaar, E. and Heath, J. K. (1992) MK: a pluripotential embryonic stem cell-derived neuroregulatory factor. Development 116, 1175-1183.
87. Patthy, L. and Nikolics, K. (1993) Functions of agrin and agrin-related proteins. Trends Neurosci. 16, 76-81.
88. Peng, H. B., Ali, A. A., Dai, Z., Daggett, D. F., Raulo, E. and Rauvala, H. (1995) The role of heparin-binding growth-associated molecule (HB-GAM) in the postsynaptic induction in cultured muscle cells. J. Neurosci. 15, 3027-3038.
89. Pittman, R. N., Ivins, J. K. and Buettner, H. M. (1989) Neuronal plasminogen activators: cell surface binding sites and involvement in neurite outgrowth. J. Neurosci. 9, 4269-4286.
90. 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.
91. Rakic, P. (1971) Guidance of neurons migrating to the fetal monkey neocortex. Brain Res. 33, 471-476.
92. Rakic, P. (1995) A small step for the cell, a giant leap for the mankind: a hypothesis of neocortical expansion during evolution. Trends Neurosci. 18, 383-388.
93. Raulo, E., Julkunen, I., Merenmies, J., Pihlaskari, R. and Rauvala, H. (1992) Secretion and biological activities of heparin-binding growth-associated molecule: neurite outgrowth-promoting and mitogenic actions of the recombinant and tissue-derived protein. J. biol. Chem. 267, 11408-11416.
94. Raulo, E., Chernousov, M. A., Carey, D. J., Nolo, R. and Rauvala, H. (1994) Isolation of a neuronal cell surface receptor of heparin binding growth-associated molecule (HB-GAM): identification as N-syndecan (syndecan-3). J. biol. Chem. 269, 12999-13004.
95. Rauvala, H. (1989) An 18 kDa heparin-binding protein of developing brain that is distinct from fibroblast growth factors. EMBO J. 8, 2933-2941.
96. 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.
97. Rauvala, H., Vanhala, A., Castrén, E., Nolo, R., Raulo, E., Merenmies, J. and Panula, P. (1994) Expression of HB-GAM (heparin-binding growth-associated molecule) in the pathways of developing axonal processes in vivo and HB-GAM-induced neurite outgrowth in vitro. Dev. Brain Res. 79, 157-176.
98. Reichardt, L. F. and Tomaselli, K. J. (1991) Extracellular matrix molecules and their receptors: functions in neural development. Annu. Rev. Neurosci. 14, 531-570.
99. Rifkin, D. B. and Moscatelli, D. (1989) Recent developments in the cell biology of basic fibroblast growth factor. J. Cell Biol. 109, 1-6.
100. Rogalski, T. M., Williams, B. D., Mullen, G. P. and Moerman, D. G. (1993) Products of the une-52 gene in Caenorhabditis elegans are homologous to the core protein of the mammalian basement membrane heparan sulfate proteoglycan. Genes Dev. 1, 1471-1484.
101. Ruoslahti, E. (1988) Structure and biology of proteoglycans. Annu. Rev. Cell Biol. 4, 229-255.
102. Ruoslahti, E. and Yamaguchi, Y. (1991) Proteoglycans as modulators of growth factor activities. Cell 64, 867-869.
103. Rupp, F., Payan, D. G., Magill-Solc, C., Cowan, D. M. and Scheller, R. H. (1991) Structure and expression of a rat agrin. Neuron 6, 811-823.
104. Saito, M., Nguyen, J. and Kidokoro, Y. (1993) Inhibition of nerve- and agrin-induced acetylcholine receptor clustering on Xenopus muscle cells in culture. Dev. Brain Res. 71, 9-17.
105. Saksela, O. and Rifkin, D. B. (1988) Cell-associated plasminogen activation: regulation and physiological functions. Annu. Rev. Cell Biol. 4, 93-126.
106. Saksela, O. and Rifkin, D. B. (1990) Release of basic fibroblast growth factor-heparan sulfate complexes from endothelial cells by plasminogen activator-mediated proteolytic activity. J. Cell Biol. 110, 767-775.
107. Salpeter, M. M. and Loring, R. H. (1985) Nicotinic acetylcholine receptors in vertebrate muscle: properties, distribution and neural control. Progr. Neurobiol. 25, 297-325.
108. Schlessinger, J., Lax, I. and Lemmon, M. (1995) Regulation of growth factor activation by proteoglycans: what is the role of the low affinity receptors?. Cell 83, 357-360.
109. Seeds, N. W., Haffke, S. P., Hawkins, R. L., Krystosek, A., McGuire, P. G. and Verrall, S. (1992) Neuronal growth cones: battering rams or lasers? In: The Nerve Growth Cone, pp. 219-229. Eds P. C. Letourneau, S. B. Kater and E. R. Macagno. Raven Press: New York.
110. Sekiguchi, K., Yokota, C., Asashima, M., Kaname, T., Fan, Q.-W., Muramatsu, T. and Kadomatsu, K. (1996) Restricted expression of Xenopus midkine gene during early development. J. Biochem. 118, 94-100.
111. Shatz, C. J., Ghosh, A., McConnell, S. K., Allendoerfer, K. L., Friauf, E. and Antonini, A. (1990) Pioneer neurons and target selection in cerebral cortical development. Cold Spring Harbor Symp. Quant. Biol. 55, 469-480.
112. Sheppard, A. M., Hamilton, S. K. and Pearlman, A. L. (1991) Changes in the distribution of extracellular matrix components accompany early morphogenetic events in mammalian cortical development. J. Neurosci. 11, 3928-3942.
113. Smalheiser, N. R. and Kim, E. (1995) Purification of cranin, a laminin binding membrane protein. Identity with dystroglycan and reassessment of its carbohydrate moieties. J. biol. Chem. 270, 15425-15433.
114. Stone, D. M. and Nikolics, K. (1995) Tissue- and age-specific expression patterns of alternatively spliced agrin mRNA transcripts in embryonic rat suggest novel developmental roles. J. Neurosci. 15, 6767-6778.
115. Sugiyama, J., Bowen, D. C. and Hall, Z. W. (1994) Dystroglycan binds nerve and muscle agrin. Neuron 13, 103-115.
116. Swenarchuk, L. E., Champaneria, S. and Anderson, M. J. (1990) Induction of a specialized muscle basal lamina at chimaeric synapses in culture. Development 110, 51-61.
117. Szabat, E. and Rauvala, H. (1996) Role of HB-GAM (heparin-binding growth-associated molecule) in proliferation arrest in cells of the developing rat limb and its expression in the differentiating neuromuscular system. Dev. Biol. 178, 77-89.
118. Tabin, C. (1991) Retinoids, homeoboxes, and growth factors: toward molecular models of limb development. Cell 66, 199-217.
119. Takeda, A., Onodera, H., Sugimoto, A., Itoyama, Y., Kogure, K., Rauvala, H. and Shibabara, S. (1995) Induction of heparin-binding growth-associated molecule (HB-GAM)expression in reactive astrocytes following hippocampal neuronal injury. Neuroscience 68, 57-64.
120. Tezuka, K.-i., Takeshita, S., Hakeda, Y., Kumegawa, M., Kikuno, R. and Hashimoto-Gotoh, T. (1990) Isolation of mouse and human cDNA clones encoding a protein expressed specifically in osteoblasts and brain tissues. Biochem. biophys. Res. Commun. 173, 246-251.
121. Tickle, C. (1995) Vertebrate limb development. Curr. Op. Genet. Dev. 5, 478-484.
122. Tsen, G., Halfter, W., Kroger, S. and Cole, G. J. (1995) Agrin is a heparan sulfate proteoglycan. J. biol. Chem. 270, 3392-3399.
123. Tsim, K. W. K., Ruegg, M. A., Escher, G., Kröger, S. and McMahan, U. J. (1992) cDNA that encodes active agrin. Neuron 8, 677-689.
124. Tsujimura, A., Yasojima, K., Kuboki, Y., Suzuki, A., Naoto, U., Shiokawa, K. and Hashimoto-Gotoh, T. (1995) Developmental and differential regulations in gene expression of Xenopus pleiotrophic factors-α and -β. Biochem. Biophys. Res. Commun. 214, 432-439.
125. Urios, P., Duprez, D., Le Caer, J.-P., Courtois, Y., Vigny, M. and Laurent, M. (1991) Molecular cloning of RI-HB, a heparin binding protein regulated by retinoic acid. Biochem. Biophys. Res. Commun. 175, 617-624.
126. Valenzuela, D. M., Stitt, T. N., DiStefano, P. S., Rojas, E., Mattsson, K., Compton, D. L., Nuñez, L., Park, J. S., Stark, J. L., Gies, D. R., Thomas, S., Le Beau, M, M., Fernald, A. A., Copeland, N. G., Jenkins, N. A., Burden, S. J., Glass, D. J. and Yancopoulos, G. D. (1995) Receptor tyrosine kinase specific for the skeletal muscle lineage: expression in embryonic muscle, at the neuromuscular junction, and after injury. Neuron 15, 573-584.
127. Vanderwinden, J. M., Mailleux, P., Schiffmann, S. N. and Vanderhaegen, J. J. (1992) Cellular distribution of the new growth factor pleiotrophin (HB-GAM) mRNA in developing rat tissues. Anal. Embryol. 186, 387-406.
128. Vigny, M., Raulais, D., Puzenat, N., Duprez, D., Hartmann, M. P., Jeanny, J. C. and Courtois, Y. (1988) Identification of a new heparin-binding protein localized within chicken basement membranes. Eur. J. Biochem. 186, 733-740.
129. Walker, A., Turnbull, J. E. and Gallagher, J. T. (1994) Specific heparan sulfate saccharides mediate the activity of basic fibroblast growth factor. J. biol. Chem. 269, 931-935.
130. Wanaka, A., Carroll, S. L. and Milbrandt, J. (1993) Develomentally regulated expression of pleiotrophin, a novel heparin binding growth factor, in the nervous system of the rat. Dev. Brain Res. 72, 133-144.
131. Wang, L. and Denburg, J. L. (1992) A role for proteoglycans in the guidance of a subset of pioneer axons in cultured embryos of the cockroach. Neuron 8, 701-714.
132. Wewetzer, K., Rauvala, H. and Unsicker, K. (1995) Immunocytochemical localization of heparin-binding growth-associated molecule (HB-GAM) in the developing and adult rat cerebellar cortex. Brain Res. 693, 31-38.
133. Wisniewski, T., Lalowski, M., Baumann, M., Rauvala, H., Raulo, E., Nolo, R. and Frangione, B. (1996) HB-GAM is a cytokine present in Alzheimer's and Down's syndrome lesions. NeuroReport 7, 667-671.
134. Yanagishita, M. and Hascall, V. C. (1992) Cell surface heparan sulfate proteoglycans. J. biol. Chem. 267, 9451-9454.
135. Yankner, B. A. (1996) Mechanisms of neuronal degeneration in Alzheimer's disease. Neuron 16, 921-932.
136. Yauon, A., Klagsbrun, M., Esko, J. P., Leder, P. and Ornitz, D. M. (1991) Cell surface, heparin-like molecules are required for binding of basic fibroblast growth factor to its high affinity receptor. Cell 64, 841-848.