The chondroitin sulfate proteoglycans neurocan, brevican, phosphacan, and versican are differentially regulated following spinal cord injury

Experimental Neurology

Volumn 182, Issue 2, 2003, Pages 399-411

  Jones, Leonard L ^a,b   Margolis, Richard U ^c   Tuszynski, Mark H ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b VA SAN DIEGO HEALTHCARE SYSTEM   (United States)

^c NEW YORK UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Astrocyte; CNS injury; CSPG; Extracellular matrix; Inhibition; Regeneration

Indexed keywords

BREVICAN; GLIAL FIBRILLARY ACIDIC PROTEIN; NEUROCAN; PHOSPHACAN; PROTEOCHONDROITIN SULFATE; UNCLASSIFIED DRUG; VERSICAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY LABELING; ARTICLE; ASTROCYTE; CELL FUNCTION; CELL LABELING; CONTROLLED STUDY; EXTRACELLULAR MATRIX; FEMALE; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; IN VIVO STUDY; NONHUMAN; PARENCHYMA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SYNTHESIS; RAT; SPINAL CORD INJURY; TISSUE LEVEL;

EID: 0042665641     PISSN: 00144886     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0014-4886(03)00087-6     Document Type: Article

References (45)

1. 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., Fawcett J.W. Neurocan is upregulated in injured brain and in cytokine-treated astrocytes. J. Neurosci. 20:2000;2427-2438.
2. Asher R.A., Morgenstern D.A., Shearer M.C., Adcock K.H., Pesheva P., Fawcett J.W. Versican is upregulated in CNS injury and is a product of oligodendrocyte lineage cells. J. Neurosci. 22:2002;2225-2236.
3. Bradbury E.J., Moon L.D., Popat R.J., King V.R., Bennett G.S., Patel P.N., Fawcett J.W., McMahon S.B. Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature. 416:2002;636-640.
4. Braunewell K.H., Pesheva P., McCarthy J.B., Furcht L.T., Schmitz B., Schachner M. Functional involvement of sciatic nerve-derived versican- and decorin-like molecules and other chondroitin sulphate proteoglycans in ECM-mediated cell adhesion and neurite outgrowth. Eur. J. Neurosci. 7:1995;805-814.
5. Bu J., Akhtar N., Nishiyama A. Transient expression of the NG2 proteoglycan by a subpopulation of activated macrophages in an excitotoxic hippocampal lesion. Glia. 34:2001;296-310.
6. Davies S.J., Fitch M.T., Memberg S.P., Hall A.K., Raisman G., Silver J. Regeneration of adult axons in white matter tracts of the central nervous system. Nature. 390:1997;680-683.
7. Dou C.L., Levine J.M. Inhibition of neurite growth by the NG2 chondroitin sulfate proteoglycan. J. Neurosci. 14:1994;7616-7628.
8. Fidler P.S., Schuette K., Asher R.A., Dobbertin A., Thornton S.R., Calle-Patino Y., Muir E., Levine J.M., Geller H.M., Rogers J.H., Faissner A., Fawcett J.W. Comparing astrocytic cell lines that are inhibitory or permissive for axon growth the major axon-inhibitory proteoglycan is NG2 . J. Neurosci. 19:1999;8778-8788.
9. Fitch M.T., Silver J. Activated macrophages and the blood-brain barrier inflammation after CNS injury leads to increases in putative inhibitory molecules . Exp. Neurol. 148:1997;587-603.
10. Geisert E.E., Bidanset D.J., Del Mar N., Robson J.A. Up-regulation of a keratan sulfate proteoglycan following cortical injury in neonatal rats. Int. J. Dev. Neurosci. 14:1996;257-267.
11. Geisert E.E., Williams R.C., Bidanset D.J. A CNS specific proteoglycan associated with astrocytes in rat optic nerve. Brain Res. 571:1992;165-168.
12. Grill R., Murai K., Blesch A., Gage F.H., Tuszynski M.H. Cellular delivery of neurotrophin-3 promotes corticospinal axonal growth and partial functional recovery after spinal cord injury. J. Neurosci. 17:1997;5560-5572.
13. Haas C.A., Rauch U., Thon N., Merten T., 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.
14. Hirsch S., Bahr M. Immunocytochemical characterization of reactive optic nerve astrocytes and meningeal cells. Glia. 26:1999;36-46.
15. Jaworski D.M., Kelly G.M., Hockfield S. Intracranial injury acutely induces the expression of the secreted isoform of the CNS-specific hyaluronan-binding protein BEHAB/brevican. Exp. Neurol. 157:1999;327-337.
16. Jones L.L., Tuszynski M.H. Spinal cord injury elicits expression of keratan sulfate proteoglycans by macrophages, reactive microglia, and oligodendrocyte progenitors. J. Neurosci. 22:2002;4611-4624.
17. Jones L.L., Yamaguchi Y., Stallcup W.B., 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.
18. Keirstead H.S., Levine J.M., Blakemore W.F. Response of the oligodendrocyte progenitor cell population (defined by NG2 labelling) to demyelination of the adult spinal cord. Glia. 22:1998;161-170.
19. Lemons M.L., Howland D.R., Anderson D.K. Chondroitin sulfate proteoglycan immunoreactivity increases following spinal cord injury and transplantation. Exp. Neurol. 160:1999;51-65.
20. Lemons M.L., Sandy J.D., Anderson D.K., Howland D.R. Intact aggrecan and fragments generated by both aggrecanse and metalloproteinase-like activities are present in the developing and adult rat spinal cord and their relative abundance is altered by injury. J. Neurosci. 21:2001;4772-4781.
21. Levine J.M. Increased expression of the NG2 chondroitin-sulfate proteoglycan after brain injury. J. Neurosci. 14:1994;4716-4730.
22. Maurel P., Rauch U., Flad M., Margolis R.K., Margolis R.U. Phosphacan, a chondroitin sulfate proteoglycan of brain that interacts with neurons and neural cell-adhesion molecules, is an extracellular variant of a receptor-type protein tyrosine phosphatase. Proc. Natl. Acad. Sci. USA. 91:1994;2512-2516.
23. McKeon R.J., Jurynec M.J., Buck C.R. The chondroitin sulfate proteoglycans neurocan and phosphacan are expressed by reactive astrocytes in the chronic CNS glial scar. J. Neurosci. 19:1999;10778-10788.
24. McTigue D.M., Wei P., Stokes B.T. Proliferation of NG2-positive cells and altered oligodendrocyte numbers in the contused rat spinal cord. J. Neurosci. 21:2001;3392-3400.
25. Milev P., Friedlander D.R., Sakurai T., Karthikeyan L., Flad M., Margolis R.K., Grumet M., Margolis R.U. Interactions of the chondroitin sulfate proteoglycan phosphacan, the extracellular domain of a receptor-type protein tyrosine phosphatase, with neurons, glia, and neural cell adhesion molecules. J. Cell Biol. 127:1994;1703-1715.
26. Moon L.D., Asher R.A., Rhodes K.E., Fawcett J.W. Regeneration of CNS axons back to their target following treatment of adult rat brain with chondroitinase ABC. Nat. Neurosci. 4:2001;465-466.
27. Moon L.D., Asher R.A., Rhodes K.E., Fawcett J.W. Relationship between sprouting axons, proteoglycans and glial cells following unilateral nigrostriatal axotomy in the adult rat. Neuroscience. 109:2002;101-117.
28. Nishiyama A., Dahlin K.J., Prince J.T., Johnstone S.R., Stallcup W.B. The primary structure of NG2, a novel membrane-spanning proteoglycan. J. Cell Biol. 114:1991;359-371.
29. Ong W.Y., Levine J.M. A light and electron microscopic study of NG2 chondroitin sulfate proteoglycan-positive oligodendrocyte precursor cells in the normal and kainate-lesioned rat hippocampus. Neuroscience. 92:1999;83-95.
30. Pasterkamp R.J., Anderson P.N., Verhaagen J. Peripheral nerve injury fails to induce growth of lesioned ascending dorsal column axons into spinal cord scar tissue expressing the axon repellent Semaphorin3A. Eur. J. Neurosci. 13:2001;457-471.
31. Plant G.W., Bates M.L., Bunge M.B. Inhibitory proteoglycan immunoreactivity is higher at the caudal than the rostral Schwann cell graft-transected spinal cord interface. Mol. Cell. Neurosci. 17:2001;471-487.
32. Powell E.M., Geller H.M. Dissection of astrocyte-mediated cues in neuronal guidance and process extension. Glia. 26:1999;73-83.
33. Redwine J.M., Armstrong R.C. In vivo proliferation of oligodendrocyte progenitors expressing PDGFalphaR during early remyelination. J. Neurobiol. 37:1998;413-428.
34. Schmalfeldt M., Bandtlow C.E., Dours-Zimmermann M.T., Winterhalter K.H., Zimmermann D.R. Brain derived versican V2 is a potent inhibitor of axonal growth. J. Cell Sci. 113:2000;807-816.
35. Schnell L., Fearn S., Klassen H., Schwab M.E., Perry V.H. Acute inflammatory responses to mechanical lesions in the CNS differences between brain and spinal cord . Eur. J. Neurosci. 11:1999;3648-3658.
36. Schnell L., Fearn S., Schwab M.E., Perry V.H., Anthony D.C. Cytokine-induced acute inflammation in the brain and spinal cord. J. Neuropathol. Exp. Neurol. 58:1999;245-254.
37. Stichel C.C., Niermann H., D'Urso D., Lausberg F., Hermanns S., Muller H.W. Basal membrane-depleted scar in lesioned CNS characteristics and relationships with regenerating axons . Neuroscience. 93:1999;321-333.
38. Streit W.J., Semple-Rowland S.L., Hurley S.D., Miller R.C., Popovich P.G., Stokes B.T. Cytokine mRNA profiles in contused spinal cord and axotomized facial nucleus suggest a beneficial role for inflammation and gliosis. Exp. Neurol. 152:1998;74-87.
39. Thon N., Haas C.A., Rauch U., Merten T., Fassler R., Frotscher M., 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.
40. Ughrin Y.M., Chen Z.J., Levine J.M. Multiple regions of the NG2 proteoglycan inhibit neurite growth and induce growth cone collapse. J. Neurosci. 23:2003;175-186.
41. Weidner N., Ner A., Salimi N., Tuszynski M.H. Spontaneous corticospinal axonal plasticity and functional recovery after adult central nervous system injury. Proc. Natl. Acad. Sci. USA. 98:2001;3513-3518.
42. Wu Y.P., Siao C.J., Lu W., Sung T.C., Frohman M.A., Milev P., Bugge T.H., Degen J.L., Levine J.M., Margolis R.U., Tsirka S.E. The tissue plasminogen activator (tPA)/plasmin extracellular proteolytic system regulates seizure-induced hippocampal mossy fiber outgrowth through a proteoglycan substrate. J. Cell Biol. 148:2000;1295-1304.
43. Yamada H., Fredette B., Shitara K., Hagihara K., Miura R., Ranscht B., Stallcup W.B., Yamaguchi Y. The brain chondroitin sulfate proteoglycan brevican associates with astrocytes ensheathing cerebellar glomeruli and inhibits neurite outgrowth from granule neurons. J. Neurosci. 17:1997;7784-7795.
44. Yamaguchi Y. Chondroitin sulfate proteoglycans in the nervous system. Iozzo R.V. Proteoglycans Structure, Biology, and Molecular Interactions . 2000;379-402 Marcel Dekker, Inc, New York.
45. Zhang Y., Tohyama K., Winterbottom J.K., Haque N.S., Schachner M., Lieberman A.R., Anderson P.N. Correlation between putative inhibitory molecules at the dorsal root entry zone and failure of dorsal root axonal regeneration. Mol. Cell. Neurosci. 17:2001;444-459.