Chondroitin/Dermatan Sulfates in the Central Nervous System: Their Structures and Functions in Health and Disease

Advances in Pharmacology

Volumn 53, Issue , 2006, Pages 337-356

  Rauch, Uwe ^a   Kappler, Joachim ^b  

^a LUND UNIVERSITY   (Sweden)

^b UNIVERSITY OF BONN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CHONDROITIN SULFATE; DERMATAN SULFATE;

ANIMAL; BRAIN; BRAIN INJURY; BRAIN LEVEL; CHEMISTRY; EPILEPSY; HUMAN; IMMUNOHISTOCHEMISTRY; METABOLISM; NEURITE; PHYSIOLOGY; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; BRAIN; BRAIN CHEMISTRY; BRAIN INJURIES; CHONDROITIN SULFATES; DERMATAN SULFATE; EPILEPSY; HUMANS; IMMUNOHISTOCHEMISTRY; NEURITES; SIGNAL TRANSDUCTION;

EID: 33846135124     PISSN: 10543589     EISSN: None     Source Type: Book Series    
DOI: 10.1016/S1054-3589(05)53016-3     Document Type: Review

References (103)

1. Ameye L., and Young M.F. Mice deficient in small leucine-rich proteoglycans: Novel in vivo models for osteoporosis, osteoarthritis, Ehlers-Danlos syndrome, muscular dystrophy, and corneal diseases. Glycobiology 12 (2002) 107R-116R
2. Asher R.A., Morgenstern D.A., Fidler P.S., Adcock K.H., Oohira A., Braistead J.E., Levine J.M., Margolis R.U., Rogers J.H., and Fawcett J.W. Neurocan is upregulated in injured brain and in cytokine-treated astrocytes. J. Neurosci. 20 (2000) 2427-2438
3. Asher R.A., Morgenstern D.A., Shearer M.C., Adcock K.H., Pesheva P., and Fawcett J.W. Versican is upregulated in CNS injury and is a product of oligodendrocyte lineage cells. J. Neurosci. 22 (2002) 2225-2236
4. Atoji Y., Yamamoto Y., and Suzuki Y. The presence of chondroitin sulfate A and C within axon terminals in the superior olivary nuclei of the adult dog. Neurosci Lett. 189 (1995) 39-42
5. Atoji Y., Yamamoto Y., Suzuki Y., Matsui F., and Oohira A. Immunohistochemical localization of neurocan in the lower auditory nuclei of the dog. Hear. Res. 110 (1997) 200-208
6. Bandtlow C.E., and Zimmermann D.R. Proteoglycans in the developing brain: New conceptual insights for old proteins. Physiol. Rev. 80 (2000) 1267-1290
7. Bao X., Nishimura S., Mikami T., Yamada S., Itoh N., and Sugahara K. Chondroitin sulfate/dermatan sulfate hybrid chains from embryonic pig brain, which contain a higher proportion of L-iduronic acid than those from adult pig brain, exhibit neuritogenic and growth factor binding activities. J. Biol. Chem. 279 (2004) 9765-9776
8. Bao X., Mikami T., Yamada S., Faissner A., Muramatsu T., and Sugahara K. Heparin-binding growth factor, pleiotrophin, mediates neuritogenic activity of embryonic pig brain-derived chondroitin sulfate/dermatan sulfate hybrid chains. J. Biol. Chem. 280 (2005) 9180-9191
9. Bekku Y., Su W.D., Hirakawa S., Fässler R., Ohtsuka A., Kang J.S., Sanders J., Murakami T., Ninomiya Y., and Oohashi T. Molecular cloning of Bral2, a novel brain-specific link protein, and immunohistochemical colocalization with brevican in perineuronal nets. Mol. Cell Neurosci. 24 (2003) 148-159
10. Bradbury E.J., Moon L.D., Popat R.J., King V.R., Bennett G.S., Patel P.N., Fawcett J.W., and McMahon S.B. Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature 416 (2002) 636-640
11. Brakebusch C., Seidenbecher C.I., Asztely F., Rauch U., Matthies H., Meyer H., Krug M., Bockers T.M., Zhou X., Kreutz M.R., Montag D., Gundelfinger E.D., et al. Brevican-deficient mice display impaired hippocampal CA1 long-term potentiation but show no obvious deficits in learning and memory. Mol. Cell Biol. 22 (2002) 7417-7427
12. Brittis P.A., and Silver J. Exogenous glycosaminoglycans induce complete inversion of retinal ganglion cell bodies and their axons within the retinal neuroepithelium. Proc. Natl. Acad. Sci. USA 91 (1994) 7539-7542
13. Burkart T., and Wiesmann U.N. Sulfated glycosaminoglycans (GAG) in the developing mouse brain. Quantitative aspects on the metabolism of total and individual sulfated GAG in vivo. Dev. Biol. 120 (1987) 447-456
14. Caggiano A.O., Zimber M.P., Ganguly A., Blight A.R., and Gruskin E.A. Chondroitinase ABCI improves locomotion and bladder function following contusion injury of the rat spinal cord. J. Neurotrauma 22 (2005) 226-239
15. Camand E., Morel M.P., Faissner A., Sotelo C., and Dusart I. Long-term changes in the molecular composition of the glial scar and progressive increase of serotoninergic fibre sprouting after hemisection of the mouse spinal cord. Eur. J. Neurosci. 20 (2004) 1161-1176
16. Castillo G.M., Lukito W., Wight T.N., and Snow A.D. The sulfate moieties of glycosaminoglycans are critical for the enhancement of beta-amyloid protein fibril formation. J. Neurochem. 72 (1999) 1681-1687
17. Celio M.R., and Blümcke I. Perineuronal nets: A specialized form of extracellular matrix in the adult nervous system. Brain Res. Brain Res. Rev. 19 (1994) 128-145
18. Chung K.Y., Taylor J.S., Shum D.K., and Chan S.O. Axon routing at the optic chiasm after enzymatic removal of chondroitin sulfate in mouse embryos. Development 127 (2000) 2673-2683
19. Chung K.Y., Shum D.K., and Chan S.O. Expression of chondroitin sulfate proteoglycans in the chiasm of mouse embryos. J. Comp. Neurol. 417 (2000) 153-163
20. Clarris H.J., Rauch U., and Key B. Dynamic spatiotemporal expression patterns of neurocan and phosphacan indicate diverse roles in the developing and adult mouse olfactory system. J. Comp. Neurol. 423 (2000) 99-111
21. Coster L., Malmstrom A., Sjoberg I., and Fransson L. The co-polymeric structure of pig skin dermatan sulphate: Distribution of L-iduronic acid sulphate residues in co-polymeric chains. Biochem. J. 145 (1975) 379-389
22. Deller T., Haas C.A., and Frotscher M. Reorganization of the rat fascia dentata after a unilateral entorhinal cortex lesion. Role of the extracellular matrix. Ann. N.Y. Acad. Sci. 911 (2000) 207-220
23. Dergham P., Ellezam B., Essagian C., Avedissian H., Lubell W.D., and McKerracher L. Rho signaling pathway targeted to promote spinal cord repair. J. Neurosci. 22 (2002) 6570-6577
24. Edgell C.J., BaSalamah M.A., and Marr H.S. Testican-1: A differentially expressed proteoglycan with protease inhibiting activities. Int. Rev. Cytol. 236 (2004) 101-122
25. Emerling D.E., and Lander A.D. Inhibitors and promoters of thalamic neuron adhesion and outgrowth in embryonic neocortex: Functional association with chondroitin sulfate. Neuron 17 (1996) 1089-1100
26. Fernaud-Espinosa I., Nieto-Sampedro M., and Bovolenta P. Differential effects of glycosaminoglycans on neurite outgrowth from hippocampal and thalamic neurones. J. Cell Sci. 107 (1994) 1437-1448
27. Flaccus A., Janetzko A., Tekotte H., Margolis R.K., and Margolis R.U. Immunocytochemical localization of chondroitin and chondroitin 4- and 6-sulfates in developing rat cerebellum. J. Neurochem. 56 (1991) 1608-1615
28. Franken S., Junghans U., Rosslenbroich V., Baader S.L., Hoffmann R., Gieselmann V., Viebahn C., and Kappler J. Collapsin response mediator proteins of neonatal rat brain interact with chondroitin sulfate. J. Biol. Chem. 278 (2003) 3241-3250
29. Grako K.A., Ochiya T., Barritt D., Nishiyama A., and Stallcup W.B. PDGF (alpha)-receptor is unresponsive to PDGF-AA in aortic smooth muscle cells from the NG2 knockout mouse. J. Cell Sci. 112 (1999) 905-915
30. Grimpe B., and Silver J. A novel DNA enzyme reduces glycosaminoglycan chains in the glial scar and allows microtransplanted dorsal root ganglia axons to regenerate beyond lesions in the spinal cord. J. Neurosci. 24 (2004) 1393-1397
31. Haas C.A., Rauch U., Thon N., Merten T., and Deller T. Entorhinal cortex lesion in adult rats induces the expression of the neuronal chondroitin sulfate proteoglycan neurocan in reactive astrocytes. J. Neurosci. 19 (1999) 9953-9963
32. Harroch S., Furtado G.C., Brueck W., Rosenbluth J., Lafaille J., Chao M., Buxbaum J.D., and Schlessinger J. A critical role for the protein tyrosine phosphatase receptor type Z in functional recovery from demyelinating lesions. Nat. Genet. 32 (2002) 411-414
33. Hasenöhrl R.U., Frisch C., Junghans U., Muller H.W., and Huston J.P. Facilitation of learning following injection of the chondroitin sulfate proteoglycan biglycan into the vicinity of the nucleus basalis magnocellularis. Behav. Brain Res. 70 (1995) 59-67
34. Heck N., Garwood J., Loeffler J.P., Larmet Y., and Faissner A. Differential upregulation of extracellular matrix molecules associated with the appearance of granule cell dispersion and mossy fiber sprouting during epileptogenesis in a murine model of temporal lobe epilepsy. Neuroscience 129 (2004) 309-324
35. Hikino M., Mikami T., Faissner A., Vilela-Silva A.C., Pavao M.S., and Sugahara K. Oversulfated dermatan sulfate exhibits neurite outgrowth-promoting activity toward embryonic mouse hippocampal neurons: Implications of dermatan sulfate in neuritogenesis in the brain. J. Biol. Chem. 278 (2003) 43744-43754
36. Huston J.P., Weth K., De Souza Silva A., Junghans U., Müller H.W., and Hasenöhrl R.U. Facilitation of learning and long-term ventral pallidal-cortical cholinergic activation by proteoglycan biglycan and chondroitin sulfate C. Neuroscience 100 (2000) 355-361
37. Inman D.M., and Steward O. Ascending sensory, but not other long-tract axons, regenerate into the connective tissue matrix that forms at the site of a spinal cord injury in mice. J. Comp. Neurol. 462 (2003) 431-449
38. Jones L.L., Margolis R.U., and Tuszynski M.H. The chondroitin sulfate proteoglycans neurocan, brevican, phosphacan, and versican are differentially regulated following spinal cord injury. Exp. Neurol. 182 (2003) 399-411
39. Jones L.L., Sajed D., and Tuszynski M.H. Axonal regeneration through regions of chondroitin sulfate proteoglycan deposition after spinal cord injury: A balance of permissiveness and inhibition. J. Neurosci. 23 (2003) 9276-9288
40. Jones L.L., Yamaguchi Y., Stallcup W.B., and Tuszynski M.H. NG2 is a major chondroitin sulfate proteoglycan produced after spinal cord injury and is expressed by macrophages and oligodendrocyte progenitors. J. Neurosci. 22 (2002) 2792-2803
41. Junghans U., Koops A., Westmeyer A., Kappler J., Meyer H.E., and Müller H.W. Purification of a meningeal cell-derived chondroitin sulphate proteoglycan with neurotrophic activity for brain neurons and its identification as biglycan. Eur. J. Neurosci. 7 (1995) 2341-2350
42. Kantor D.B., Chivatakarn O., Peer K.L., Oster S.F., Inatani M., Hansen M.J., Flanagan J.G., Yamaguchi Y., Sretavan D.W., Giger R.J., and Kolodkin A.L. Semaphorin 5A is a bifunctional axon guidance cue regulated by heparan and chondroitin sulfate proteoglycans. Neuron 44 (2004) 961-975
43. Kappler J., Junghans U., Koops A., Stichel C.C., Hausser H.J., Kresse H., and Müller H.W. Chondroitin/dermatan sulphate promotes the survival of neurons from rat embryonic neocortex. Eur. J. Neurosci. 9 (1997) 306-318
44. Kappler J., Stichel C.C., Gleichmann M., Gillen C., Junghans U., Kresse H., and Müller H.W. Developmental regulation of decorin expression in postnatal rat brain. Brain Res. 793 (1998) 328-332
45. Katoh-Semba R., Matsuda M., Watanabe E., Maeda N., and Oohira A. Two types of brain chondroitin sulfate proteoglycan: Their distribution and possible functions in the rat embryo. Neurosci. Res. 31 (1998) 273-282
46. Kitagawa H., Tsutsumi K., Tone Y., and Sugahara K. Developmental regulation of the sulfation profile of chondroitin sulfate chains in the chicken embryo brain. J. Biol. Chem. 272 (1997) 31377-31381
47. Kobayashi K., Takahashi M., Matsushita N., Miyazaki J., Koike M., Yaginuma H., Osumi N., Kaibuchi K., and Kobayashi K. Survival of developing motor neurons mediated by Rho GTPase signaling pathway through Rho-kinase. J. Neurosci. 24 (2004) 3480-3488
48. Lafont F., Rouget M., Triller A., Prochiantz A., and Rousselet A. In vitro control of neuronal polarity by glycosaminoglycans. Development 114 (1992) 17-29
49. Lafont F., Prochiantz A., Valenza C., Petitou M., Pascal M., Rouget M., and Rousselet A. Defined glycosaminoglycan motifs have opposite effects on neuronal polarity in vitro. Dev. Biol. 165 (1994) 453-468
50. Lemons M.L., Howland D.R., and Anderson D.K. Chondroitin sulfate proteoglycan immunoreactivity increases following spinal cord injury and transplantation. Exp. Neurol. 160 (1999) 51-65
51. Lander A.D. Proteoglycans: Master regulators of molecular encounter?. Matrix Biol. 17 (1998) 465-472
52. Leung K.M., Taylor J.S., and Chan S.O. Enzymatic removal of chondroitin sulphates abolishes the age-related axon order in the optic tract of mouse embryos. Eur. J. Neurosci. 17 (2003) 1755-1767
53. Leung K.M., Margolis R.U., and Chan S.O. Expression of phosphacan and neurocan during early development of mouse retinofugal pathway. Brain Res. Dev. Brain Res. 152 (2004) 1-10
54. Lips K., Stichel C.C., and Müller H.W. Restricted appearance of tenascin and chondroitin sulphate proteoglycans after transection and sprouting of adult rat postcommissural fornix. J. Neurocytol. 24 (1995) 449-464
55. Maeda N., He J., Yajima Y., Mikami T., Sugahara K., and Yabe T. Heterogeneity of the chondroitin sulfate portion of phosphacan/6B4 proteoglycan regulates its binding affinity for pleiotrophin/heparin binding growth-associated molecule. J. Biol. Chem. 278 (2003) 35805-35811
56. Margolis R.K., Margolis R.U., Preti C., and Lai D. Distribution and metabolism of glycoproteins and glycosaminoglycans in subcellular fractions of brain. Biochemistry 14 (1975) 4797-4804
57. Margolis R.U., Margolis R.K., Chang L.B., and Preti C. Glycosaminoglycans of brain during development. Biochemistry 14 (1975) 85-88
58. Matsui F., Kawashima S., Shuo T., Yamauchi S., Tokita Y., Aono S., Keino H., and Oohira A. Transient expression of juvenile-type neurocan by reactive astrocytes in adult rat brains injured by kainate-induced seizures as well as surgical incision. Neuroscience 112 (2002) 773-781
59. Matthews R.T., Kelly G.M., Zerillo C.A., Gray G., Tiemeyer M., and Hockfield S. Aggrecan glycoforms contribute to the molecular heterogeneity of perineuronal nets. J. Neurosci. 22 (2002) 7536-7547
60. Meyer-Puttlitz B., Junker E., Margolis R.U., and Margolis R.K. Chondroitin sulfate proteoglycans in the developing central nervous system. II. Immunocytochemical localization of neurocan and phosphacan. J. Comp. Neurol. 366 (1996) 44-54
61. Miller B., Sheppard A.M., Bicknese A.R., and Pearlman A.L. Chondroitin sulfate proteoglycans in the developing cerebral cortex: The distribution of neurocan distinguishes forming afferent and efferent axonal pathways. J. Comp. Neurol. 355 (1995) 615-628
62. Mjaatvedt C.H., Yamamura H., Capehart A.A., Turner D., and Markwald R.R. The Cspg2 gene, disrupted in the hdf mutant, is required for right cardiac chamber and endocardial cushion formation. Dev. Biol. 202 (1998) 56-66
63. Monnier P.P., Sierra A., Schwab J.M., Henke-Fahle S., and Mueller B.K. The Rho/ROCK pathway mediates neurite growth-inhibitory activity associated with the chondroitin sulfate proteoglycans of the CNS glial scar. Mol. Cell Neurosci. 22 (2003) 319-330
64. Moon L.D., Asher R.A., Rhodes K.E., and Fawcett J.W. Relationship between sprouting axons, proteoglycans and glial cells following unilateral nigrostriatal axotomy in the adult rat. Neuroscience 109 (2002) 101-117
65. Morawski M., Bruckner M.K., Riederer P., Bruckner G., and Arendt T. Perineuronal nets potentially protect against oxidative stress. Exp. Neurol. 188 (2004) 309-315
66. Murakami T., and Ohtsuka A. Perisynaptic barrier of proteoglycans in the mature brain and spinal cord. Arch. Histol. Cytol. 66 (2003) 195-207
67. Naffah-Mazzacoratti M.G., Arganaraz G.A., Porcionatto M.A., Scorza F.A., Amado D., Silva R., Bellissimo M.I., Nader H.B., and Cavalheiro E.A. Selective alterations of glycosaminoglycans synthesis and proteoglycan expression in rat cortex and hippocampus in pilocarpine-induced epilepsy. Brain Res. Bull. 50 (1999) 229-239
68. Nandini C.D., Itoh N., and Sugahara K. Novel 70-kDa chondroitin sulfate/dermatan sulfate hybrid chains with a unique heterogeneous sulfation pattern from shark skin, which exhibit neuritogenic activity and binding activities for growth factors and neurotrophic factors. J. Biol. Chem. 280 (2005) 4058-4069
69. Nandini C.D., Mikami T., Ohta M., Itoh N., Akiyama-Nambu F., and Sugahara K. Structural and functional characterization of oversulfated chondroitin sulfate/dermatan sulfate hybrid chains from the notochord of hagfish. Neuritogenic and binding activities for growth factors and neurotrophic factors. J. Biol. Chem. 279 (2004) 50799-50809
70. Perosa S.R., Porcionatto M.A., Cukiert A., Martins J.R., Amado D., Nader H.B., Cavalheiro E.A., Leite J.P., and Naffah-Mazzacoratti M.G. Extracellular matrix components are altered in the hippocampus, cortex, and cerebrospinal fluid of patients with mesial temporal lobe epilepsy. Epilepsia 43 Suppl 5 (2002) 159-161
71. Perosa S.R., Porcionatto M.A., Cukiert A., Martins J.R., Passeroti C.C., Amado D., Matas S.L., Nader H.B., Cavalheiro E.A., Leite J.P., and Naffah-Mazzacoratti M.G. Glycosaminoglycan levels and proteoglycan expression are altered in the hippocampus of patients with mesial temporal lobe epilepsy. Brain Res. Bull. 58 (2002) 509-516
72. Pizzorusso T., Medini P., Berardi N., Chierzi S., Fawcett J.W., and Maffei L. Reactivation of ocular dominance plasticity in the adult visual cortex. Science 298 (2002) 1248-1251
73. Probstmeier R., Stichel C.C., Müller H.W., Asou H., and Pesheva P. Chondroitin sulfates expressed on oligodendrocyte-derived tenascin-R are involved in neural cell recognition. Functional implications during CNS development and regeneration. J. Neurosci. Res. 60 (2000) 21-36
74. Properzi F., Carulli D., Asher R.A., Muir E., Camargo L.M., van Kuppevelt T.H., ten Dam G.B., Furukawa Y., Mikami T., Sugahara K., Toida T., Geller H.M., and Fawcett J.W. Chondroitin 6-sulphate synthesis is up-regulated in injured CNS, induced by injury-related cytokines and enhanced in axon-growth inhibitory glia. Eur. J. Neurosci. 21 (2005) 378-390
75. Rauch U., Glössl J., and Kresse H. Comparison of small proteoglycans from skin fibroblasts and vascular smooth-muscle cells. Biochem. J. 238 (1986) 465-474
76. Rauch U., Gao P., Janetzko A., Flaccus A., Hilgenberg L., Tekotte H., Margolis R.K., and Margolis R.U. Isolation and characterization of developmentally regulated chondroitin sulfate and chondroitin/keratan sulfate proteoglycans of brain identified with monoclonal antibodies. J. Biol. Chem. 266 (1991) 14785-14801
77. Rauch U., Hirakawa S., Oohashi T., Kappler J., and Roos G. Cartilage link protein interacts with neurocan, which shows hyaluronan binding characteristics different from CD44 and TSG-6. Matrix Biol. 22 (2004) 629-639
78. Rolls A., Avidan H., Cahalon L., Schori H., Bakalash S., Litvak V., Lev S., Lider O., and Schwartz M. A disaccharide derived from chondroitin sulphate proteoglycan promotes central nervous system repair in rats and mice. Eur. J. Neurosci. 20 (2004) 1973-1983
79. Salinero O., Moreno-Flores M.T., and Wandosell F. Increasing neurite outgrowth capacity of beta-amyloid precursor protein proteoglycan in Alzheimer's disease. J. Neurosci. Res. 60 (2000) 87-97
80. Sasaki T., Mann K., and Timpl R. Modification of the laminin alpha 4 chain by chondroitin sulfate attachment to its N-terminal domain. FEBS Lett. 505 (2001) 173-178
81. Sasaki T., Mann K., Miner J.H., Miosge N., and Timpl R. Domain IV of mouse laminin beta1 and beta2 chains. Eur. J. Biochem. 269 (2002) 431-442
82. Schnepp A., Komp Lindgren P., Hulsmann H., Kroger S., Paulsson M., and Hartmann U. Mouse testican-2: Expression, glycosylation and effects on neurite outgrowth. J. Biol. Chem. 280 (2005) 11274-11280
83. Shuo T., Aono S., Matsui F., Tokita Y., Maeda H., Shimada K., and Oohira A. Developmental changes in the biochemical and immunological characters of the carbohydrate moiety of neuroglycan C, a brain-specific chondroitin sulfate proteoglycan. Glycoconj. J. 20 (2004) 267-278
84. Silver J., and Miller J.H. Regeneration beyond the glial scar. Nat. Rev. Neurosci. 5 (2004) 146-156
85. Sivasankaran R., Pei J., Wang K.C., Zhang Y.P., Shields C.B., Xu X.M., and He Z. PKC mediates inhibitory effects of myelin and chondroitin sulfate proteoglycans on axonal regeneration. Nat. Neurosci. 7 (2004) 261-268
86. Snow A.D., Mar H., Nochlin D., Kresse H., and Wight T.N. Peripheral distribution of dermatan sulfate proteoglycans (decorin) in amyloid-containing plaques and their presence in neurofibrillary tangles of Alzheimer's disease. J. Histochem. Cytochem. 40 (1992) 105-113
87. Snow D.M., Atkinson P.B., Hassinger T.D., Letourneau P.C., and Kater S.B. Chondroitin sulfate proteoglycan elevates cytoplasmic calcium in DRG neurons. Dev. Biol. 166 (1994) 87-100
88. Sobel R.A., and Ahmed A.S. White matter extracellular matrix chondroitin sulfate/dermatan sulfate proteoglycans in multiple sclerosis. J. Neuropathol. Exp. Neurol. 60 (2001) 1198-1207
89. Stichel C.C., Kappler J., Junghans U., Koops A., Kresse H., and Muller H.W. Differential expression of the small chondroitin/dermatan sulfate proteoglycans decorin and biglycan after injury of the adult rat brain. Brain Res. 704 (1995) 263-274
90. Sykova E. Glial diffusion barriers during aging and pathological states. Prog. Brain Res. 132 (2001) 339-363
91. Tang X., Davies J.E., and Davies S.J. Changes in distribution, cell associations, and protein expression levels of NG2, neurocan, phosphacan, brevican, versican V2, and tenascin-C during acute to chronic maturation of spinal cord scar tissue. J. Neurosci. Res. 71 (2003) 427-444
92. Thon N., Haas C.A., Rauch U., Merten T., Fässler R., Frotscher M., and Deller T. The chondroitin sulphate proteoglycan brevican is upregulated by astrocytes after entorhinal cortex lesions in adult rats. Eur. J. Neurosci. 12 (2000) 2547-2558
93. Tsuchida K., Shioi J., Yamada S., Boghosian G., Wu A., Cai H., Sugahara K., and Robakis N.K. Appican, the proteoglycan form of the amyloid precursor protein, contains chondroitin sulfate E in the repeating disaccharide region and 4-O-sulfated galactose in the linkage region. J. Biol. Chem. 276 (2001) 37155-37160
94. Uchimura K., Kadomatsu K., Nishimura H., Muramatsu H., Nakamura E., Kurosawa N., Habuchi O., El-Fasakhany F.M., Yoshikai Y., and Muramatsu T. Functional analysis of the chondroitin 6-sulfotransferase gene in relation to lymphocyte subpopulations, brain development, and oversulfated chondroitin sulfates. J. Biol. Chem. 277 (2002) 1443-1450
95. Ughrin Y.M., Chen Z.J., and Levine J.M. Multiple regions of the NG2 proteoglycan inhibit neurite growth and induce growth cone collapse. J. Neurosci. 23 (2003) 175-186
96. von-Koch C.S., Zheng H., Chen H., Trumbauer M., Thinakaran G., van der Ploeg L.H., Price D.L., and Sisodia S.S. Generation of APLP2 KO mice and early postnatal lethality in APLP2/APP double KO mice. Neurobiol. Aging 18 (1997) 661-669
97. Vorisek I., Hajek M., Tintera J., Nicolay K., and Sykova E. Water ADC, extracellular space volume, and tortuosity in the rat cortex after traumatic injury. Magn. Reson. Med. 48 (2002) 994-1003
98. Watanabe H., Kimata K., Line S., Strong D., Gao L.Y., Kozak C.A., and Yamada Y. Mouse cartilage matrix deficiency (cmd) caused by a 7 bp deletion in the aggrecan gene. Nat. Genet. 7 (1994) 154-157
99. Yick L.W., Cheung P.T., So K.F., and Wu W. Axonal regeneration of Clarke's neurons beyond the spinal cord injury scar after treatment with chondroitinase ABC. Exp. Neurol. 182 (2003) 160-168
100. Yick L.W., So K.F., Cheung P.T., and Wu W.T. Lithium chloride reinforces the regeneration-promoting effect of chondroitinase ABC on rubrospinal neurons after spinal cord injury. J. Neurotrauma 21 (2004) 932-943
101. Zheng H., Jiang M., Trumbauer M.E., Sirinathsinghji D.J., Hopkins R., Smith D.W., Heavens R.P., Dawson G.R., Boyce S., Conner M.W., Stevens K.A., Slunt H.H., et al. Beta-amyloid precursor protein-deficient mice show reactive gliosis and decreased locomotor activity. Cell 81 (1995) 525-531
102. Zhou X.H., Brakebusch C., Matthies H., Oohashi T., Hirsch E., Moser M., Krug M., Seidenbecher C.I., Boeckers T.M., Rauch U., Buettner R., Gundelfinger E.D., et al. Neurocan is dispensable for brain development. Mol. Cell Biol. 21 (2001) 5970-5978
103. Zou P., Zou K., Muramatsu H., Ichihara-Tanaka K., Habuchi O., Ohtake S., Ikematsu S., Sakuma S., and Muramatsu T. Glycosaminoglycan structures required for strong binding to midkine, a heparin-binding growth factor. Glycobiology 13 (2003) 35-42