Heparan sulfate proteoglycans in the nervous system: Their diverse roles in neurogenesis, axon guidance, and synaptogenesis

Seminars in Cell and Developmental Biology

Volumn 12, Issue 2, 2001, Pages 99-106

  Yamaguchi, Yu ^a  

^a BURNHAM INSTITUTE   (United States)

Author keywords

Axon guidance; Dendritic spine; Heparan sulfate proteoglycan; Neurogenesis; Synapse

Indexed keywords

CELL SURFACE RECEPTOR; FIBROBLAST GROWTH FACTOR 2; FIBROBLAST GROWTH FACTOR RECEPTOR; GLYCOSYLTRANSFERASE; GLYPICAN; PERLECAN; PLEIOTROPHIN; PROTEOHEPARAN SULFATE; SYNDECAN;

ANIMAL CELL; BONE DEVELOPMENT; CELL ADHESION; CELL MIGRATION; CELL TYPE; DENDRITE; DENDRITIC SPINE; EMBRYO DEVELOPMENT; HEREDITARY MULTIPLE EXOSTOSIS; HUMAN; HUMAN CELL; NERVE CELL DIFFERENTIATION; NERVE FIBER; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SYNTHESIS; REGULATORY MECHANISM; REVIEW; STEM CELL; SYNAPTOGENESIS;

MAMMALIA;

EID: 0035782881     PISSN: 10849521     EISSN: None     Source Type: Journal    
DOI: 10.1006/scdb.2000.0238     Document Type: Article

References (65)

1. Yamaguchi Y (2000) Chondroitin sulfate proteoglycans in the nervous system, in Proteoglycans: Structure, Biology and Molecular Interactions (Iozzo R, ed.) pp. 379-402. Marcel Dekker Inc, New York
2. Margolis RU, Margolis RK (1997) Chondroitin sulfate proteoglycans as mediators of axon growth and pathfinding. Cell Tissue Res 290:343-348
3. Perrimon N, Bernfield M (2000) Specificities of heparan sulfate proteoglycans in developmental processes. Nature 404:725-728
4. Bandtlow CE, Zimmermann DR (2000) Proteoglycans in the developing brain: New conceptual insights for old proteins. Physiol Rev 80:1267-1290
5. McKay R (1997) Stem cells in the central nervous system. Science 276:66-71
6. Powell PP, Finkelstein SP, Dionne CA, Jaye M, Klagsbrun M (1991) Temporal, differential and regional expression of mRNA for basic fibroblast growth factor in the developing and adult rat brain. Mol Brain Res 11:71-77
7. Giordano S, Sherman L, Lyman W, Morrison R (1992) Multiple molecular weight forms of basic fibroblast growth factor are developmentally regulated in the central nervous system. Dev Biol 152:293-303
8. Weiss B, Janet T, Grothe C (1993) Localization of bFGF and FGF-receptors in the developing nervous system of the embryonic and newborn rat. J Neurosci Res 34:442-453
9. Qian X, Davis AA, Goderie SK, Temple S (1997) FGF2 concentration regulates the generation of neurons and glia from multipotent cortical stem cells. Neuron 18:81-93
10. Ghosh A, Greenberg ME (1995) Distinct roles for bFGF and NT-3 in the regulation of cortical neurogenesis. Neuron 15:89-103
11. Vicario-Abajón C, Johe KK, Hazel TG, Collazo D, McKay RDG (1995) Functions of basic fibroblast growth factor and neurotrophins in the differentiation of hippocampal neurons. Neuron 15:105-114
12. Ornitz DM (2000) FGFs, heparan sulfate and FGFRs: Complex interactions essential for development. Bioessays 22:108-112
13. Watanabe K, Yamada H, Yamaguchi Y (1995) K-glypican: A novel heparan sulfate proteoglycan that is highly expressed in developing brain and kidney. J Cell Biol 130:1207-1218
14. Hagihara K, Watanabe K, Chun J, Yamaguchi Y (2000) Glypican-4 is an FGF2-binding heparan sulfate proteoglycan expressed in neural precursor cells. Dev Dyn (in press)
15. Altman J, Das GD (1965) Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J Comp Neurol 124:319-335
16. Litwack ED, Ivins JK, Kimbasar A, Paine-Saunders S, Stipp CS, Lander AD (1998) Expression of the heparan sulfate proteoglycan glypican-1 in the developing rodent. Dev Biol 211:72-87
17. Litwack ED, Stipp CS, Kimbasar A, Lander AD (1994) Neuronal expression of glypican-1, a cell-surface glycosylphosphatidylinositol-anchored heparan sulfate proteoglycan, in the adult rat nervous system. J Neurosci 14:3713-3724
18. Stipp CS, Litwack ED, Lander AD (1993) 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
19. Ivins JK, Litwack ED, Kumbasar A, Stipp CS, Lander AD (1997) Cerebroglycan, a developmentally regulated cell-surface heparan sulfate proteoglycan, is expressed on developing axons and growth cones. Dev Biol 184:320-332
20. Saunders S, Paine-Saunders S, ad Lander AD (1997) Expression of the cell surface proteoglycan glypican-5 is developmentally regulated in kidney, limb, and brain. Dev Biol 190:78-93
21. Aviezer D, Hecht D, Safran M, Eisinger M, David G, Yayon A (1994) Perlecan, basal lamina proteoglycan, promotes basic fibroblast growth factor-receptor binding, mitogenesis, and angiogenesis. Cell 79:1005-1013
22. Nurcombe V, Ford MD, Wildschut JA, Bartlett PF (1993) Developmental regulation of neural response to FGF-1 and FGF-2 by heparan sulfate proteoglycan. Science 260:103-106
23. Joseph SJ, Ford MD, Barth C, Portbury S, Bartlett PF, Nurcombe V, Greferath U (1996) A proteoglycan that activates fibroblast growth factors during early neuronal development is a perlecan variant. Development 122:3443-3453
24. McCormick C, Leduc Y, Martindale D, Mattison K, Esford LE, Dyer AP, Tufaro F (1998) The putative tumour suppressor EXT1 alters the expression of cell-surface heparan sulfate. Nat Genet 19:158-161
25. Lind T, Tufaro F, McCormick C, Linadhl U, Lindholt K (1998) The putative tumor suppressors EXT1 and EXT2 are glycosyltransferases required for the biosynthesis for heparan sulfate. J Biol Chem 273:26265-26268
26. Wang L, Denburg JL (1992) A role for proteoglycans in the guidance of a subset of pioneer axons in cultured embryos of the cockroach. Neuron 8:7701-7714
27. Rajan I, Denburg JL (1997) Mesoderm guidance of pioneer axon growth. Dev Biol 190:214-228
28. Walz A, McFarlane S, Brickman YG, Nurcombe V, Bartlett PF, Holt CE (1997) Essential role of heparan sulfates in axon navigation and targeting in the developing visual system. Development 124:2421-2430
29. McFarlane S, McNeill L, Holt CE (1995) FGF signaling and target recognition in the developing Xenopus visual system. Neuron 15:1017-1028
30. McFarlane S, Cornel E, Amaya E, Holt CE (1996) Inhibition of FGF receptor activity in retinal ganglion cell axons causes errors in target recognition. Neuron 17:245-254
31. Nyhus JK, Denburg JL (1998) The in vivo regulation of pioneer axon growth by FGF-2 and heparan sulfate proteoglycans in cultured embryos of the cockroach. Mol Cell Neurosci 11:305-323
32. Raulo E, Chernousov MA, Carey DJ, Nolo R, 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
33. Kinnunen A, Kinnunen T, Kaksonen M, Nolo R, Panula P, Rauvala H (1998) N-syndecan and HB-GAM (heparin-binding growth-associated molecule) associate with early axonal tracts in the rat brain. Eur J Neurosci 10:635-648
34. Kinnunen A, Niemi M, Kinnunen T, Kaksonen M, Nolo R, Rauvala H (1999) Heparan sulfate and HB-GAM (heparin-binding growth-associated molecule) in the development of the thalamocortical pathway of rat brain. Eur J Neurosci 11:491-502
35. Bondareff W (1967) An intercellular substance in rat cerebral cortex: Submicroscopic distribution of ruthenium red. Anat Rec 157:527-535
36. Tani E, Ametani T (1971) Extracellular distribution of ruthenium red-positive substance in the cerebral cortex. J Ultrastruct Res 34:1-14
37. Eldridge CF, Sanes JR, Chiu AY, Bunge RP, Cornbrooks CJ (1986) Basal lamina-associated heparan sulphate proteoglycan in the rat PNS: Characterization and localization using monoclonal antibodies. J Neurocytol 15:37-51
38. Cole GJ, Halfter W (1996) Agrin: An extracellular matrix heparan sulfate proteoglycan involved in cell interactions and synaptogenesis. Perspect Dev Neurobiol 3:359-371
39. Meier T, Masciulli F, Moore C, Schoumacher F, Eppenberger U, Denzer AJ, Jones G, Brenner HR (1998) Agrin can mediate acetylcholine receptor gene expression in muscle by aggregation of muscle-derived neuregulins. J Cell Biol 141:715-726
40. Harris KM, Kater SB (1994) Dendritic spines: Cellular specializations imparting both stability and flexibility to synaptic function. Annu Rev Neurosci 17:341-371
41. Ziv NE, Smith SJ (1996) Evidence for a role of dendritic filopodia in synaptogenesis and spine formation. Neuron 17:91-102
42. Crick F (1982) Do dendritic spines twitch? Trends Neurosci 5:44-46
43. Calverley RKS, Jones DG (1990) Contributions of dendritic spines and perforated synapses to synaptic plasticity. Brain Res Brain Res Rev 15:215-249
44. Buchs P-A, Muller D (1996) Induction of long-term potentiation is associated with major ultrastructural changes of activated synapses. Proc Natl Acad Sci USA 93:8040-8045
45. Engert F, Bonhoeffer T (1999) Dendritic spine changes associated with hippocampal long-term synaptic plasticity. Nature 39:66-70
46. Fifková E (1985) A possible mechanism of morphometric changes in dendritic spines induced by stimulation. Cell Mol Neurobiol 5:47-63
47. Wisniewski KE, Segan SM, Miezejeski CM, Sersen EA, Rudelli RD (1991) The Fra(X) syndrome: Neurological, electrophysiological, and neuropathological abnormalities. Am J Med Genet 38:476-480
48. Cohen AR, Wood DF, Marfatia SM, Walther Z, Chishti AH, Anderson JM (1998) Human CASK/LIN-2 binds syndecan-2 and protein 4.1 and localizes to the basolateral membrane of epithelial cells. J Cell Biol 142:129-138
49. Hsueh YP, Yang FC, Kharazia V, Naisbitt S, Cohen AR, Weinberg RJ, Sheng M (1998) Direct interaction of CASK/LIN-2 and syndecan heparan sulfate proteoglycan and their overlapping distribution in neuronal synapses. J Cell Biol 142:139-151
50. Ethell IM, Yamaguchi Y (1999) Cell surface heparan sulfate proteoglycan syndecan-2 induces the maturation of dendritic spines in rat hippocampal neurons. J Cell Biol 144:575-586
51. Grootjans JJ, Zimmermann P, Reekmans G, Smets A, Degeest G, Durr J, David G (1997) Syntenin, a PDZ protein that binds syndecan cytoplasmic domains. Proc Natl Acad Sci USA 94:13683-13688
52. Gao Y, Li M, Simons M (2000) Synectin, syndecan-4 cytoplasmic domain binding PDZ protein, inhibits cell migration. J Cell Physiol 184:373-379
53. Ethell IM, Hagihara K, Miura Y, Irie F, Yamaguchi Y (2000) Synbindin, a novel syndecan-2-binding protein in neuronal dendritic spines. J Cell Biol 151:53-67
54. Torres R, Firestein BL, Dong H, Sraudinger J, Olson EN, Huganir RL, Bredt DS, Gale NW, Yancopoulos GD (1998) PDZ proteins bind, cluster, and synaptically colocalize with Eph receptors and their ephrin ligands. Neuron 21:1453-1463
55. Asundi VK, Carey DJ (1997) Phosphorylation of recombinant N-syndecan (syndecan 3) core protein. Biochem Biophys Res Commun 240:502-506
56. Reiland J, Ott VL, Lebakken CS, Yeaman C, McCarthy J, Rapraeger AC (1996) Pervanadate activation of intracellular kinases leads to tyrosine phosphorylation and shedding of syndecan-1. Biochem J 319:39-47
57. Oh ES, Couchman JR, Woods A (1995) Serine phosphorylation of syndecan-2 proteoglycan cytoplasmic domain. Arch Biochem Biophys 344:67-74
58. Itano N, Oguri K, Nagayasu Y, Kusano Y, Nakanishi H, David G, Okayama M (1996) Phosphorylation of a membrane-intercalated proteoglycan, syndecan-2 expressed in stroma-inducing clone from a mouse Lewis lung carcinoma. Biochem J 315:925-930
59. David G, Bai XM, Van der Schueren B, Marynen P, Cassiman J-J, Van der Berghe H (1993) Spatial and temporal changes in the expression of fibroglycan (syndecan-2) during mouse embryonic development. Development 119:841-854
60. Carey DJ, Stahl RC, Tucker B, Bendt KA, Cizmeci-Smith G (1994) Aggregation-induced association of syndecan-1 with microfilaments mediated by the cytoplasmic domain. Exp Cell Res 214:12-21
61. Woods A, Couchman JR (1994) Syndecan-4 heparan sulfate proteoglycan is a selectively enriched and widespread focal adhesion component. Mol Biol Cell 5:183-192
62. Carey DJ, Bendt KM, Stahl RC (1996) The cytoplasmic domain of syndecan-1 is required for cytoskeleton association but not detergent insolubility. Identification of essential cytoplasmic domain residues. J Biol Chem 271:15253-15260
63. Lauri SE, Kaukinen S, Kinnenen T, Vlinen A, Imai S, Kaila K, Taira T, Rauvala H (1999) Regulatory role and molecular interactions of a cell-surface heparan sulfate proteoglycan (N-syndecan) in hippocampal long-term potentiation. J Neurosci 19:1226-1235
64. Lin X, Shi Z, Dryer L, Esko JD, Wells DE, Matzuk MM (2000) Disruption of gastrulation and heparan sulfate biosynthesis in EXT1-deficient mice. Dev Biol 224:299-311
65. Ramon y Cajal S (1995) Histology of the Nervous System of Man and Vertebrates. Oxford University Press, New York