The chondroitin sulfate proteoglycans neurocan and phosphacan are expressed by reactive astrocytes in the chronic CNS glial scar

Journal of Neuroscience

Volumn 19, Issue 24, 1999, Pages 10778-10788

  McKeon, Robert J ^a   Jurynec, Michael J ^a   Buck, Charles R ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Axonal regeneration; Chondroitin sulfate proteoglycans; CNS injury; Gene expression; Glial scars; Reactive astrocytes

Indexed keywords

CHONDROITIN SULFATE; COMPLEMENTARY DNA; PROTEOGLYCAN; RNA;

ANIMAL CELL; ARTICLE; ASTROCYTE; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; GENE EXPRESSION; GLIA CELL; NERVE CELL CULTURE; NERVE FIBER REGENERATION; NERVOUS SYSTEM INJURY; NEWBORN; NONHUMAN; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCAR FORMATION;

EID: 0033573386     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.19-24-10778.1999     Document Type: Article

References (68)

1. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389-3402.
2. Ascher RA, Fidler PS, Rogers, JH, Fawcett JW (1998) TGF-β stimulates neurocan synthesis in cultured rat astrocytes. Soc Neurosci Abstr 24:56.
3. Bicknese AR, Sheppard AM, O'Leary DM, Pearlman AL (1994) Thalamocortical axons extend along a chondroitin sulfate proteoglycan-enriched pathway coincident with the neocortical subplate and distinct from the efferent path. J Neurosci 14:3500-3510.
4. Bovolenta P, Wandosell F, Nieto-Sampedro M (1993) Characterization of a neurite outgrowth inhibitor expressed after CNS injury. Eur J Neurosci 5:454-465.
5. Bovolenta P, Fernaud-Espinosa I, Méndez-Otero R, Nieto-Sampedro M (1997) Neurite outgrowth inhibitor of gliotic brain tissue. Mode of action and cellular localization, studied with specific monoclonal antibodies. Eur J Neurosci 9:977-989.
6. Chomezynski P, Sacchi N (1987) Single step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162:156-159.
7. Clarke SR, Shetty AK, Bradley JL, Turner DA (1994) Reactive astrocytes express the embryonic intermediate neurofilament nestin. NeuroReport 5:1885-1888.
8. Davies S, Field PM, Raisman G (1996) Regeneration of cut adult axons fails even in the presence of continuous aligned glial pathways. Exp Neurol 142:203-216.
9. Davies S, 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.
10. 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.
11. Dou CL, Levine JM (1994) Inhibition of neurite growth by the NG2 chondroitin sulfate proteoglycan. J Neurosci 14:7616-7628.
12. Dou CL, Levine JM (1995) Differential effects of glycosaminoglycans on neurite growth on laminin and L1 substrates. J Neurosci 15:8053-8066.
13. 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.
14. 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.
15. Freeman RS, Estus S, Johnson EM (1994) Analysis of cell cycle-related gene expression in postmitotic neurons: selective induction of cyclin D1 during programmed cell death. Neuron 12:343-355.
16. Friedlander D, Milev P, Karthikeyan, 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.
17. Frisén J, Johansson CB, Török C, Risling M, Lendahl U (1995) Rapid, widespread, and long lasting induction of nestin contributes to the generation of glial scar tissue after CNS injury. J Cell Biol 131:453-464.
18. Garwood J, Schnädelbach O, Clement A, Schütte K, Bach A, Faissner A (1999) DSD-1-proteoglycan is the mouse homolog of phosphacan and displays opposing effects on neurite outgrowth dependent on neuronal lineage. J Neurosci 19:3888-3899.
19. Quo M, Dow KE, Kisilevsky R, Riopelle RJ (1993) Novel neurite growth-inhibitory properties of an astrocyte proteoglycan. J Chem Neuroanat 6:239-245.
20. Herndon ME, Lander AD (1990) A diverse set of developmentally regulated proteoglycans is expressed in the rat central nervous system. Neuron 4:949-961.
21. Hori O, Brett J, Slattery T, Cao R, Zhang J, Chen JX, Nagashima M, Lundh ER, Vijay S, Nitecki D, Morser J, Stern D, Schmitt A (1995) The receptor for advanced glycation end products (RAGE) is a cellular binding site for amphoterin. Mediation of neurite outgrowth and coexpression of rage and amphoterin in the developing nervous system. J Biol Chem 270:25752-25761.
22. Imai Y, Ibaraki K, Odajima R, Shishiba Y (1994) Analysis of proteoglycan synthesis by retro-ocular tissue fibroblasts under the influence of interleukin-1β and transforming growth factor-β. Eur J Endocrinol 131:630-638.
23. Jaworski DM, Kelly GM, Hockfield S (1999) Intracranial injury acutely induces the expression of the secreted isoform of the CNS-specific hyaluronan-binding protein BEHAB/brevican. Exp Neurol 157:327-337.
24. Jin C-F, Mata M, Fink DJ (1994) Rapid construction of deleted DNA fragments for use as internal standards in competitive PCR. PCR Methods Appl 3:252-255.
25. Knuckey NW, Finch P, Palm DE, Primiano MJ, Johanson CE, Flanders KC, Thompson NL (1996) Differential neuronal and astrocytic expression of transforming growth factor beta isoforms in rat hippocampus following transient forebrain ischemia. Mol Brain Res 40:1-14.
26. Krieglstein K, Rufer M, Suter-Crazzolara C, Unsicker K (1995) Neural functions of the transforming growth factors beta. Int J Dev Neurosci 13:301-315.
27. Levine JM (1994) Increased expression of the NG2 chondroitin-sulfate proteoglycan after brain injury. J Neurosci 14:4716-4730.
28. Lewis SA, Balcarek JM, Krek V, Shelanski M, Cowan NJ (1984) Sequence of a cDNA clone encoding mouse glial fibrillary acidic protein: structural conservation of intermediate filaments. Proc Natl Acad Sci USA 8:2743-2746.
29. Li Y-S, Milner PG, Chauhan AK, Watson MA, Hoffman RM, Kodner CM, Millbrandt J, Deuel TF (1990) Cloning and expression of a developmentally regulated protein that induces mitogenic and neurite outgrowth activity. Science 250:1690-1694.
30. Logan A, Frautschy SA, Gonzalez A-M, Sporn MB, Baird A (1992) Enhanced expression of transforming growth factor-β1 in the rat brain after a localized cerebral injury. Brain Res 587:216-225.
31. Ma Q, Sommer L, Cserjesi P, Anderson DJ (1997) Mash1 and neurogenin1 expression patterns define complementary domains of neuroepi-thelium in the developing CNS and are correlated with regions expressing notch ligands. J Neurosci 17:3644-3652.
32. Maeda N, Noda M (1996) 6B4 proteoglycan/phosphacan is a repulsive substratum but promotes morphological differentiation of cortical neurons. Development 122:647-658.
33. Maeda N, Hamanaka H, Oohira A, Noda M (1995) Purification, characterization and developmental expression of a brain-specific chondroitin sulfate protcoglycan, 6B4 proteoglycan/phosphacan. Neuroscience 67:23-35.
34. Maeda N, Nishiwaki T, Shintani T, Hamanaka H, Noda M (1996) 6B4 proteoglycan/phosphacan, an extracellular variant of receptor-like protein-tyrosine phosphatase zeta/RPTPbeta, binds pleiotrophin/ heparin-binding growth-associated molecule (HB-GAM). J Biol Chem 271:21446-21452.
35. Margolis RK, Margolis RU (1993) Nervous tissue proteoglycans. Experientia 49:429-446.
36. Maurel P, Rauch U, Flad M, Margolis RK, Margolis RU (1994) Phosphacan, a chondroitin sulfate proteoglycan of the brain that interacts with neurons and neural cell-adhesion molecules, is an extracellular variant of a receptor-type protein tyrosinc phosphatase. Proc Nat Acad Sci USA 91:2512-2516.
37. McCarthy KD, de Vellis J (1980) Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral tissue. J Cell Biol 85:890-902.
38. McKeon RJ, Schreiber RC, Rudge JS, Silver J (1991) Reduction of neurite outgrowth in a model of glial scarring is correlated with the expression of inhibitory molecules on reactive astrocytes. J Neurosci 11:3398-3411.
39. McKeon RJ, Höke A, Silver J (1995) Injury-induced proteoglycans inhibit the potential for laminin-mediatcd axon growth on astrocytic scars. Exp Neurol 136:32-43.
40. McKeon RJ, Silver J, Large TH (1997) Expression of full-length trkB receptors by reactive astrocytes after chronic CNS injury. Exp Neurol 148:558-567.
41. 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.
42. Meyer-Puttlitz B, Junker E, Margolis RU, Margolis RK (1996) Chondroitin sulfate proteoglycans in the developing central nervous system: Immunocytochemical localization of neurocan and phosphacan. J Comp Neurol 366:44-54.
43. Milev P, Friedlander DR, Sakurai T, Karthikeyan L, Flad M, Margolis RK, Grumet M, Margolis RU (1994) Interactions of the chondroitin sulfate protcoglycan phosphacan, the extracellular domain of a receptor-type protein tyrosine phosphatase, with neurons, glia, and neural cell adhesion molecules. J Cell Biol 127:1703-1715.
44. Milev P, Chiba A, Häring M, Rauvala H, Schachner M, Ranscht B, Margolis RK, Margolis RU (1998) High affinity binding and overlapping localization of neurocan and phosphacan protein-tyrosine phosphatase-zeta/beta with tenascin-R, amphoterin, and the heparin-binding growth-associated molecule. J Biol Chem 273:6998-7005.
45. Miller B, Sheppard AM, Bicknese AR, Pearlman AL (1995) Chondroitin sulfate proteoglycans the developing cerebral cortex: the distribution of neurocan distinguishes forming afferent and efferent axonal pathways. J Comp Neurol 355:615-628.
46. Napolitano EW, Chin SSM, Colman DR, Liem RKH (1987) Complete amino acid sequence and in vitro expression of rat NF-M, the middle molecular weight neurofilament protein. J Neurosci 7:2590-2599.
47. Nishiyama A, Lin XH, Giese N, Heldin CH, Stallcup WB (1996) Interaction between NG2 proteoglycan and PDGF alpha-receptor on O2A progenitor cells is required for optimal response to PDGF. J Neurosci Res 43:315-330.
48. Oohira A, Matsui F, Katoh-Semba R (1991) Inhibitory effects of brain chondroitin sulfate proteoglycans on neurite outgrowth from PC12 cells. J Neurosci 11:822-827.
49. Oohira A, Matsui F, Watanabe E, Kushima Y, Maeda M (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.
50. Rauch U, Karthikeyan L, Maurel P, Margolis RK, Margolis RU (1992) Cloning and primary structure of neurocan, a developmentally regulated, aggregating chondroitin sulfate proteoglycan of brain. J Biol Chem 267:19536-19547.
51. Robbins M, McKinney M (1992) Transcriptional regulation of neuromodulin (GAP-43) in mouse neuroblastoma clone N1E-115 as evaluated by the RT/PCR method. Mol Brain Res 13:83-92.
52. Rudge JS, Smith GM, Silver J (1989) An in vivo model of wound healing in the CNS: analysis of cell reaction and interaction at different ages. Exp Neurol 103:1-16.
53. Sakurai T, Friedlander DR, Grumet M (1996) Expression of polypeptide variants of receptor-type protein tyrosine phosphatase beta: the secreted form, phosphacan, increases dramatically during embryonic development and modulates glial cell behavior in vitro. J Neurosci Res 43:694-706.
54. Sakurai T, Lustig M, Nativ M, Hemperly JJ, Schlessinger J, Peles E, Grumet M (1997) Induction of neurite outgrowth through contactin and Nr-CAM by extracellular regions of glial receptor tyrosine phosphatase beta. J Cell Biol 136:907-918.
55. Schaeren-Wiemers N, Gerfin-Moser A (1993) A single protocol to detect transcripts of various types and expression levels in neural tissue and cultured cells: in situ hybridization using digoxigenin-labeled cRNA probes. Histochemistry 100:431-440.
56. Schnädelbach O, Mandl C, Faissner A (1998) Expression of DSD-1-PG in primary neural and glial-derived cell line cultures, upregulation by TGF-beta, and implications for cell-substrate interactions of the glial cell line oli-neu. Glia 23:99-119.
57. Shitara K, Yamada H, Watanabe K, Shimonaka M, Yamaguchi Y (1994) Brain-specific receptor-type protein-tyrosine phosphatase RPTP beta is a chondroitin sulfate proteoglycan in vivo. J Biol Chem 269:20189-20193.
58. Snow DM, Steindler DA, Silver J (1990a) Molecular and cellular characterization of the glial roof plate of the spinal cord and optic tectum: a possible role for proteoglycans in the development of an axon barrier. Dev Biol 138:359-376.
59. Snow DM, Lemmon V, Carrino DA, Caplan AI, Silver J (1990b) Sulfated proteoglycans in astroglial barriers inhibit neurite outgrowth in vitro. Exp Neurol 109:111-130.
60. Snow DM, Watanabe M, Letourneau PC, Silver J (1991) A chondroitin sulfate proteoglycan may influence the direction of retinal ganglion cell outgrowth. Development 113:1473-1485.
61. Snyder SE, Li J, Schauwecker PE, McNeill TH, Salton SRJ (1996) Comparison of RPTPz/β, phosphacan, and trkB mRNA expression in the developing and adult rat nervous system and induction of RPTPz/β and phosphacan mRNA following brain injury. Mol Brain Res 40:79-96.
62. Stallcup WB, Beasly L (1987) Bipotential glial precursor cells of the optic nerve express the NG2 proteoglycan. J Neurosci 7:2737-2744.
63. van der Wal EA, Gomez-Pinella F, Cotman C (1993) Transforming growth factor β1 is in plaques in Alzheimer and Down pathologies. NeuroReport 4:69-72.
64. Yaeger PC, Masi TL, De OJ, Binette F, Tubo R, McPherson JM (1997) Synergistic action of transforming growth factor-beta and insulin-like growth factor-I induces expression of type II collagen and aggrecan genes in adult human articular chondrocytes. Exp Cell Res 237:318-325.
65. Yamada H, Watanabe K, Shimonaka M, Yamaguchi Y (1994) Molecular cloning of Brevican, a novel brain proteoglycan of the Aggrecan/ Versican family. J Biol Chem 269:10119-10126.
66. Yamada H, Fredette B, Shitara K, Hagihara K, Miura R, Ranscht B, Stallcup WB, Yamaguchi Y (1997) The brain chondroitin sulfate proteoglycan brevican associates with astrocytes ensheathing cerebellar glomeruli and inhibits neurite outgrowth from granule neurons. J Neurosci 17:7784-7795.
67. Yeh HJ, He YY, Xu J, Hsu CY, Deuel T (1998) Upregulation of pleiotrophin gene expression in developing microvasculature, macrophages, and astrocytes after acute ischemic brain injury. J Neurosci 18:3699-3707.
68. Zuo J, Hernandez YJ, Muir D (1998) Chondroitin sulfate proteoglycan with neurite-inhibiting activity is up-regulated following peripheral nerve injury. J Neurobiol 34:41-54.