Neurocan is upregulated in injured brain and in cytokine-treated astrocytes

Journal of Neuroscience

Volumn 20, Issue 7, 2000, Pages 2427-2438

  Asher, Richard A ^a   Morgenstern, Daniel A ^a,b   Fidler, Penny S ^a,b   Adcock, Kathryn H ^a,b   Oohira, Atsuhiko ^c   Braistead, Janet E ^f   Levine, Joel M ^d   Margolis, Richard U ^e   Rogers, John H ^a   Fawcett, James W ^a,b  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c INSTITUTE FOR DEVELOPMENTAL RESEARCH   (Japan)

^d State University of New York ^*  (United States)

^e NEW YORK UNIVERSITY MEDICAL CENTER   (United States)

^f SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

Author keywords

Chondroitin sulfate; EGF; Extracellular matrix; Glial scar; Proteoglycan; Regeneration; TGF

Indexed keywords

CHONDROITIN SULFATE; CYTOKINE; EPIDERMAL GROWTH FACTOR; GAMMA INTERFERON; MONOCLONAL ANTIBODY; PLATELET DERIVED GROWTH FACTOR; PROTEOGLYCAN; TRANSFORMING GROWTH FACTOR BETA1;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN INJURY; CENTRAL NERVOUS SYSTEM; EXTRACELLULAR MATRIX; FEMALE; GLIA CELL; NERVE FIBER REGENERATION; NERVE REGENERATION; NONHUMAN; PRIORITY JOURNAL; RAT; SCAR FORMATION;

EID: 0034175517     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.20-07-02427.2000     Document Type: Article

References (69)

1. Asher R, Bignami A (1991) Localization of hyaluronate in primary glial cell cultures derived from newborn rat brain. Exp Cell Res 195:401-411.
2. Asher R, Perides G, Vanderhaeghen J-J, Bignami A (1991) Extracellular matrix of central nervous system white matter: demonstration of an hyaluronate-protein complex. J Neurosci Res 28:410-421.
3. Asher RA, Scheibe RJ, Keiser HD, Bignami A (1995) On the existence of a cartilage-like proteoglycan and link proteins in the centra nervous system. Glia 13:294-308.
4. Asher RA, Fidler PS, Rogers JH, Fawcett JW (1998) TGFbeta stimulates neurocan synthesis in cultured rat astrocytes. Soc Neurosci Abstr 24:56.
5. Asher RA, Morgenstern DA, Adcock KH, Rogers JH, Fawcett JW (1999) Versican is up-regulated in CNS injury and is a product of O-2A lineage cells. Soc Neurosci Abstr 25:750.
6. Aspberg A, Miura R, Bourdoulous S, Shimonaka M, Heinegård D, Schachner M, Ruoslahti E, Yamaguchi Y (1997) The C-type lectin domains of lecticans, a family of aggregating chondroitin sulfate proteoglycans, bind tenascin-R by protein-protein interactions independent of carbohydrate moiety. Proc Natl Acad Sci USA 94:10116-10121.
7. Baghdassarian D, Toru-Delbauffe D, Gavaret JM, Pierre M (1993) Effects of transforming growth factor-β1 on the extracellular matrix and cytoskeleton of cultured astrocytes. Glia 7:193-202.
8. Bähr M, Przyrembel C, Bastmeyer M (1995) Astrocytes from adult rat optic nerves are nonpermissive for regenerating retinal ganglion cell axons. Exp Neurol 131:211-220.
9. Baier H, Klostermann S (1994) Axon guidance and growth cone collapse in vitro. Neuroprotocols 4:96-105.
10. Barker RA, Dunnett SB, Faissner A, Fawcett JW (1996) The time course of loss of dopaminergic neurons and the gliotic reaction surrounding grafts of embryonic mesencephalon to the striatum. Exp Neurol 141:79-93.
11. Ben-Hur T, Rogister B, Murray K, Rougon G, Dubois-Dalcq M (1998) Growth and fate of PSA-NCAM+ precursors of the postnatal brain. J Neurosci 18:5777-5788.
12. Bovolenta P, Wandosell F, Nieto-Sampedro M (1993) Characterization of a neurite outgrowth inhibitor expressed after CNS injury. Eur J Neurosci 5:454-465.
13. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248-254.
14. Brittis PA, Silver J (1994) Exogenous glycosaminoglycans induce complete inversion of retinal ganglion cell bodies and their axons within the retinal neuroepithelium. Proc Natl Acad Sci USA 91:7539-7542.
15. Brittis PA, Canning DR, Silver J (1992) Chondroitin sulfate as a regulator of neuronal patterning in the retina. Science 255:733-736.
16. Davies SJA, Fitch MT, Memberg SP, Hall AK, Raisman G, Silver J (1997) Regeneration of adult axons in white matter tracts of the central nervous system. Nature 390:680-683.
17. Davies SJA, Goucher DR, Doller C, Silver J (1999) Robust regeneration of adult sensory axons in degenerating white matter of the adult rat spinal cord. J Neurosci 19:5810-5822.
18. Dodd J, Morton SB, Karagogeos D, Yamamoto M, Jessell TM (1988) Spatial regulation of axonal glycoprotein expression on subsets of embryonic spinal neurons. Neuron 1:105-116.
19. Dou C-L, Levine JM (1994) Inhibition of neurite growth by the NG2 chondroitin sulfate proteoglycan. J Neurosci 14:7616-7628.
20. Emerling DE, Lander AD (1996) Inhibitors and promoters of thalamic neuron adhesion and outgrowth in embryonic neocortex: functional association with chondroitin sulfate. Neuron 17:1089-1100.
21. Engel M, Maurel P, Margolis RU, Margolis RK (1996) Chondroitin sulfate proteoglycans in the developing central nervous system. I. Cellular sites of synthesis of neurocan and phosphacan. J Comp Neurol 366:34-43.
22. Fawcett JW, Asher RA (1999) The glial scar and CNS repair. Brain Res Bull 49:377-391.
23. Fawcett JW, Housden E, Smith-Thomas LC, Meyer RL (1989) The growth of axons in three-dimensional astrocyte cultures. Dev Biol 135:449-458.
24. Fichard A, Verna JM, Olivares J, Saxod R (1991) Involvement of a chondroitin sulfate proteoglycan in the avoidance of chick epidermis by dorsal root ganglia fibers: a study using β-D-xyloside. Dev Biol 148:1-9.
25. Fidler PS, Schuette K, Asher RA, Dobbertin A, Thornton SR, Calle-Patino Y, Muir E, Levine JM, Geller HM, Rogers JH, Faissner A, Fawcett JW (1999) Comparing astrocytic cells lines that are inhibitory or permissive for axon growth: the major axon-inhibitory proteoglycan is NG2. J Neurosci 19:8778-8788.
26. Friedlander DR, Milev P, Karthikeyan L, Margolis RK, Margolis RU, Grumet M (1994) The neuronal chondroitin sulfate proteoglycan neurocan binds to the neural cell adhesion molecules Ng-CAM/L1/NILE and N-CAM, and inhibits neuronal adhesion and neurite outgrowth. J Cell Biol 125:669-680.
27. Frisen J, Haegerstrand A, Risling M, Fried K, Johansson CB, Hammarberg H, Elde R, Hokfelt T, Cullheim S (1995) Spinal axons in central nervous system scar tissue are closely related to laminin-immunorcactive astrocytes. Neuroscience 65:293-304.
28. Gates MA, Fillmore H, Steindler DA (1996) Chondroitin sulfate proteoglycan and tenascin in the wounded adult mouse neostriatum in vitro: dopamine neuron attachment and process outgrowth. J Neurosci 16:8005-8018.
29. Giulian D, Baker TJ (1986) Characterization of ameboid microglia isolated from developing mammalian brain. J Neurosci 6:2163-2178.
30. Griffith RW, McKeon RJ (1999) Immunoneutralization of TGFbeta attenuates CS-PG synthesis and enhances process outgrowth in vitro and in vivo. Soc Neurosci Abstr 25:749.
31. Grill RJ, Stallcup WB, Tuszynski MH (1998) Temporal upregulation and spatial distribution of putative inhibitory and growth permissive substrate molecules in the injured adult rat spinal cord. Soc Neurosci Abstr 24:1054.
32. Grumet M, Flaccus A, Margolis RU (1993) Functional characterization of chondroitin sulfate proteoglycans of brain: interactions with neurons and neural cell adhesion molecules. J Cell Biol 120:815-824.
33. Grumet M, Milev P, Sakurai T, Karthikeyan L, Bourdon M, Margolis RK, Margolis RU (1994) Interactions with tenascin and differential effects on cell adhesion of neurocan and phosphacan, two major chondroitin sulfate proteoglycans of nervous tissue. J Biol Chem 269:12142-12146.
34. Haas CA, Rauch U, Thon N, Merten T, Deller T (1999) Entorhinal cortex lesion in adult rats induces the expression the neuronal chondroitin sulfate proteoglycan neurocan in reactive astrocytes. J Neurosci 19:9953-9963.
35. Katoh-Semba R, Matsuda M, Watanabe E, Maeda N, Oohira A (1998) Two types of brain chondroitin sulfate proteoglycan: their distribution and possible functions in the rat embryo. Neurosci Res 31:273-282.
36. Lagord C, Gonzalez AM, Clarke WE, Jackson RH, Baird A, Logan A (1999) Antagonizing TGFbeta activity in CNS wounds inhibits glial scarring. Soc Neurosci Abstr 25:749.
37. Laywell ED, Dorries U, Bartsch U, Faissner A, Schachner M, Steindler DA (1992) Enhanced expression of the developmentally regulated extracellular matrix molecule tenascin following adult brain injury. Proc Natl Acad Sci USA 89:2634-2638.
38. Le Roux PD, Reh TA (1996) Reactive astroglia support primary dendritic but not axonal outgrowth from mouse cortical neurons in vitro. Exp Neurol 137:49-65.
39. Levine JM (1994) Increased expression of the NG2 chondroitin-sulfate proteoglycan after brain injury. J Neurosci 14:4716-4730.
40. Lindholm D, Castren E, Kiefer R, Zafra F, Thoenen H (1992) Transforming growth factor-β1 in the rat brain: increase after injury and inhibition of astrocyte proliferation. J Cell Biol 117:395-400.
41. Logan A, Berry M (1993) Transforming growth factor-β1 and basic fibroblast growth factor in the injured CNS. Trends Neurosci 14:337-343.
42. Margolis RU, Margolis RK (1997) Chondroitin sulfate proteoglycans as mediators of axon growth and pathfinding. Cell Tissue Res 290:343-348.
43. Matsui F, Watanabe E, Oohira A (1994) Immunological identification of two proteoglycan fragments derived from neurocan, a brain-specific chondroitin sulfate proteoglycan. Neurochem Int 25:425-431.
44. McKeon RJ, Schreibe RC, Rudge JS, Silver J (1991) Reduction of neurite outgrowth in a model of glial scarring following CNS injury is correlated with the expression of inhibitory molecules on reactive astrocytes. J Neurosci 11:3398-3411.
45. McKeon RJ, Höke A, Silver J (1995) Injury-induced proteoglycans inhibit the potential for laminin-mediated axon growth on astrocytic scars. Exp Neurol 136:32-43.
46. Meyer-Puttlitz B, Milev P, Junker E, Zimmer I, Margolis RU, Margolis RK (1995) Chondroitin sulfate and chondroitin/keratan sulfate proteoglycans of nervous tissue: developmental changes of neurocan and phosphacan. J Neurochem 65:2327-2337.
47. Meyer-Puttlitz B, Junker E, Margolis RU, Margolis RK (1996) Chondroitin sulfate proteoglycans in the developing central nervous system. II. Immunocytochemical localization of neurocan and phosphacan. J Comp Neurol 366:44-54.
48. Milev P, Maurel P, Haring M, Margolis RK, Margolis RU (1996) TAG-1/axonin-1 is a high-affinity ligand of neurocan, phosphacan/protein-tyrosine phosphatase-ζ/β, and N-CAM. J Biol Chem 271:15716-15723.
49. Milev P, Chiba A, Häring M, Rauvala H, Schachner M, Ranscht B, Margolis RK, Margolis RU (1998a) High affinity binding and overlapping localization of neurocan and phosphacan/protein-tyrosine phosphatase-ζ/β with tenascin-R, amphoterin, and the heparin-binding growth-associated molecule. J Biol Chem 273:6998-7005.
50. Milev P, Maurel P, Chiba A, Mevissen M, Popp S, Yamaguchi Y, Margolis RK, Margolis RU (1998b) Differential regulation of expression of hyaluronan-binding proteoglycans in brain: aggrecan, versican, neurocan, and brevican. Biochem Biophys Res Commun 247:207-212.
51. Moon LDF, Rhodes K, Fawcett JW (1999) Extensive axon regeneration following in vivo treatment of rat brain the chondroitinase ABC. Soc Neurosci Abstr 25:751.
52. Noble M, Fok-Seang J, Cohen J (1984) Glia are a unique substrate for the in vitro growth of central nervous system neurons. J Neurosci 4:1892-1903.
53. Oohira A, Matsui F, Watanabe E, Kushima Y, Maeda N (1994) Developmentally regulated expression of a brain specific species of chondroitin sulfate proteoglycan, neurocan, identified with a monoclonal antibody 1G2 in the rat cerebrum. Neuroscience 60:145-157.
54. Pindzola RR, Doller C, Silver J (1993) Putative inhibitory extracellular matrix molecules at the dorsal root entry zone of the spinal cord during development and after root and sciatic nerve lesions. Dev Biol 156:34-48.
55. Plant GW, Dimitropolou A, Bates ML, Bunge MB (1998) The expression of inhibitory proteoglycans following transplantation of Schwann cell grafts into completely transected rat spinal cord. Soc Neurosci Abstr 24:69.
56. Rabchevsky AG, Weinitz JM, Coulpier M, Fages C, Tinel M, Junier M-P (1998) A role for transforming growth factor a as an inducer of astrogliosis. J Neurosci 18:10541-10552.
57. Rauch U, Gao P, Janetzko A, Flaccus A, Hilgenberg L, Tekotte H, Margolis RK, Margolis RU (1991) Isolation and characterization of developmentally regulated chondroitin sulfate and chondroitin/keratan sulfate proteoglycans of brain identified with monoclonal antibodies. J Biol Chem 266:14785-14801.
58. Rauch U, Karthikeyan L, Maurel P, Margolis RU, Margolis RK (1992) Cloning and primary structure of neurocan, a developmentally regulated, aggregating chondroitin sulfate proteoglycan of brain. J Biol Chem 267:19536-19547.
59. Rauch U, Grimpe B, Kulbe G, Arnold-Ammer I, Beier DR, Fassler R (1995) Structure and chromosomal localization of the mouse neurocan gene. Genomics 28:405-410.
60. Rauch U, Clement A, Retzler C, Frohlich L, Fassler R, Gohring W, Faissner A (1997) Mapping of a defined neurocan binding site to distinct domains of tenascin-C. J Biol Chem 272:26905-26912.
61. Smith GM, Hale JH (1997) Macrophage/microglia regulation of astrocytic tenascin: synergistic action of transforming growth factor-β and basic fibroblast growth factor. J Neurosci 17:9624-9633.
62. Smith GM, Miller RH, Silver J (1986) Changing role of forebrain astrocytes during development, regenerative failure, and induced regeneration upon transplantation. J Comp Neurol 251:23-43.
63. Smith-Thomas LC, Fok-Seang J, Stevens J, Du J-S, Muir E, Faissner A, Geller HM, Rogers JH, Fawcett JW (1994) An inhibitor of neurite outgrowth produced by astrocytes. J Cell Sci 107:1687-1695.
64. Smith-Thomas LC, Stevens J, Fok-Seang J, Faissner A, Rogers JH, Fawcett JW (1995) Increased axon regeneration in astrocytes grown in the presence of proteoglycan synthesis inhibitors. J Cell Sci 108:1307-1315.
65. Stichel CC, Kappler J, Junghans U, Koops A, Kresse H, Müller HW (1995) Differential expression of the small chondroitin/dermatan sulfate proteoglycans decorin and biglycan after injury of the adult rat brain. Brain Res 704:263-274.
66. Tuttle R, Schlaggar BL, Braisted JE, O'Leary DDM (1995) Maturation-dependent upregulation of growth-promoting molecules in developing cortical plate controls thalamic and cortical neurite growth. J Neurosci 15:3039-3052.
67. Tuttle R, Braisted JE, Richards LJ, O'Leary DDM (1998) Retinal axon guidance by region-specific cues in diencephalon. Development 125:791-801.
68. Watanabe E, Aono S, Matsui F, Yamada Y, Naruse I, Oohira A (1995) Distribution of a brain-specific proteoglycan, neurocan, and the corresponding mRNA during the formation of barrels in the rat somatosensory cortex. Eur J Neurosci 7:547-554.
69. Zuo J, Neubauer D, Dyess K, Ferguson TA, Muir D (1998) Degradation of chondroitin sulfate proteoglycan enhances the neurite-promoting potential of spinal cord tissue. Exp Neurol 154:654-662.