Entorhinal cortex lesion in adult rats induces the expression of the neuronal chondroitin sulfate proteoglycan neurocan in reactive astrocytes

Journal of Neuroscience

Volumn 19, Issue 22, 1999, Pages 9953-9963

  Haas, Carola A ^a   Rauch, Uwe ^b   Thon, Niklas ^a   Merten, Tobias ^a   Deller, Thomas ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

^b LUND UNIVERSITY HOSPITAL   (Sweden)

Author keywords

Axon growth; Extracellular matrix; Fascia dentata; Hippocampus; Plasticity; Sprouting

Indexed keywords

CELL SURFACE PROTEIN; MESSENGER RNA; NEUROCAN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN DEVELOPMENT; BRAIN INJURY; CONTROLLED STUDY; DISEASE COURSE; ENTORHINAL CORTEX; EXTRACELLULAR MATRIX; MALE; NERVE FIBER GROWTH; NERVE FIBER REGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN INDUCTION; RAT; TISSUE DISTRIBUTION;

EID: 0033571943     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.19-22-09953.1999     Document Type: Article

References (59)

1. Bicknese AR, Sheppard AM, O'Leary DD, 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.
2. Campbell KA, Bank B, Milgram NW (1984) Epileptogenic effects of electrolytic lesions in the hippocampus: role of iron deposition. Exp Neurol 86:506-514.
3. Cotman CW, Nieto-Sampedro M, Harris EW (1981) Synapse replacement in the nervous system of adult vertebrates. Physiol Rev 61:684-784.
4. Dasheiff RM, McNamara JO (1982) Electrolytic entorhinal cortex lesions cause seizures. Brain Res 231:444-450.
5. Davies SJA, Fitch MT, Memberg ST, Hall AK, Raisman G, Silver J (1997) Regeneration of adult axons in white matter tracts of the central nervous system. Nature 390:680-683.
6. 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.
7. Deller T (1998) The anatomical organization of the rat fascia dentata -new aspects of laminar organization as revealed by anterograde tracing with phaseolus vulgaris-leucoagglutinin. Anat Embryol 197:89-103.
8. Deller T, Frotscher M (1997) Lesion-induced plasticity of central neurons: sprouting of single fibers in the rat hippocampus after unilateral entorhinal lesion. Prog Neurobiol 53:687-727.
9. Deller T, Frotscher M, Nitsch R (1995) Morphological evidence for the sprouting of inhibitory commissural fibers in response to the lesion of the excitatory entorhinal input to the rat dentate gyrus. J Neurosci 15:6868-6878.
10. Deller T, Martinez A, Nitsch R, Frotscher M (1996a) A novel entorhinal projection to the rat dentate gyrus: direct innervation of proximal dendrites and cell bodies of granule cells and GABAergic neurons. J Neurosci 16:3322-3333.
11. Deller T, Nitsch R, Frotscher M (1996b) Layer-specific sprouting of commissural fibers to the rat fascia dentata after unilateral entorhinal cortex lesion: a phaseolus vulgaris leucoagglutinin tracing study. Neuroscience 71:651-660.
12. Deller T, Haas CA, Naumann T, Joester A, Faissner A, Frotscher M (1997) Upregulation of astrocyte-derived tenascin-C correlates with neurite outgrowth in the rat dentate gyrus after unilateral entorhinal cortex lesion. Neuroscience 81:829-846.
13. 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.
14. Ferhat L, Chevassus-Au-Louis N, Jorquera J, Niquet J, Khrestchatisky M, Ben-Ari Y, Represa A (1996a) Transient increase of tenascin-C in immature hippocampus: astroglial and neuronal expression. J Neurocytol 25:53-66.
15. Ferhat L, Chevassus-Au-Louis N, Khrestchatisky M, Ben-Ari Y, Represa A (1996b) Seizures induce tenascin-C mRNA expression in neurons. J Neurocytol 25:535-546.
16. 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.
17. Frotscher M, Heimrich B, Deller T (1997) Sprouting in the hippocampus is layer-specific. Trends Neurosci 20:218-223.
18. Fukuda T, Kawano H, Ohyama K, Li HP, Takeda Y, Oohira A, Kawamura K (1997) Immunohistochemical localization of neurocan and L1 in the formation of thalamocortical pathways of developing rats. J Comp Neurol 382:141-152.
19. Gall C, Rose G, Lynch G (1979) Proliferative and migratory activity of glial cells in the partially deafferented hippocampus. J Comp Neurol 183:539-550.
20. 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.
21. Grumet M, Friedlander DR, Sakurai T (1996) Functions of brain chondroitin sulfate proteoglycans during development: interactions with adhesion molecules. Perspect Dev Neurobiol 3:319-330.
22. Hailer NP, Bechmann I, Heizmann S, Nitsch R (1997) Adhesion molecule expression on phagocytic microglial cells following anterograde degeneration of perforant path axons. Hippocampus 7:341-349.
23. Höke A, Silver J (1996) Proteoglycans and other repulsive molecules in glial boundaries during development and regeneration of the nervous system. Prog Brain Res 108:149-163.
24. Katoh-Semba R, Matsuda M, Kato K, Oohira A (1995) Chondroitin sulphate proteoglycans in the rat brain: candidates for axon barriers of sensory neurons and the possible modification by laminin of their actions. Eur J Neurosci 7:613-621.
25. Kelley MS, Steward O (1996a) The process of reinnervation in the dentate gyrus of adult rats: physiological events at the time of the lesion and during the early postlesion period. Exp Neurol 139:73-82.
26. Kelley MS, Steward O (1996b) The role of postlesion seizures and spreading depression in the upregulation of glial fibrillary acidic protein mRNA after entorhinal cortex lesions. Exp Neurol 139:83-94.
27. Lee M-Y, Deller T, Kirsch M, Frotscher M, Hofmann H-D (1997) Differential regulation of ciliary neurotrophic factor (CNTF) and CNTF receptor a expression in astrocytes and neurons of the fascia dentata after entorhinal cortex lesion. J Neurosci 17:1137-1146.
28. Lips K, Stichel CC, Müller HW (1995) Restricted appearance of tenascin and chondroitin sulphate proteoglycans after transection and sprouting of adult rat postcommissural fornix. J Neurocytol 24:449-464.
29. Lynch G, Matthews DA, Mosko S, Parks T, Cotman CW (1972) Induced acetylcholinesterase-rich layer in rat dentate gyrus following entorhinal lesions. Brain Res 42:311-318.
30. Margolis RU, Margolis RK (1997) Chondroitin sulfate proteoglycans as mediators of axon growth and pathfinding. Cell Tissue Res 290:343-348.
31. Matsui F, Nishizuka M, Yasuda Y, Aono S, Watanabe E, Oohira A (1998) Occurrence of a N-terminal proteolytic fragment of neurocan, not a C-terminal half, in a perineuronal net in the adult rat cerebrum. Brain Res 790:45-51.
32. Matthews DA, Cotman CW, Lynch G (1976a) An electron microscopic study of lesion-induced synaptogenesis in the dentate gyrus of the adult rat. I. Magnitude and time course of degeneration. Brain Res 115:1-21.
33. Matthews DA, Cotman CW, Lynch G (1976b) An electron microscopic study of lesion-induced synaptogenesis in the dentate gyrus of the adult rat. II. Reappearance of morphologically normal synaptic contacts. Brain Res 115:23-41.
34. Mesulam MM, Geula C, Moràn MA (1987) Anatomy of cholinesterase inhibition in Alzheimer's disease: effect of physostigmine and tetrahydroaminoacridine on plaques and tangles. Ann Neurol 22:683-691.
35. 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.
36. Milev P, Maurel P, Haring M, Margolis RK, Margolis RU (1996) TAG-1/axonin-1 is a high-affinity ligand of neurocan, phosphacan/proteintyrosine phosphatase-zeta/beta, and N-CAM. J Biol Chem 271:15716-15723.
37. Milev P, Maurel P, Chiba A, Mevissen M, Popp S, Yamaguchi Y, Margolis RK, Margolis RU (1998) Differential regulation of expression of hyaluronan-binding proteoglycans in developing brain: aggrecan, versican, neurocan, and brevican. Biochem Biophys Res Commun 207-212.
38. Miller B, Sheppard AM, Bicknese AR, Pearlman AL (1995) Chondroitin sulfate proteoglycans in the developing cerebral cortex: the distribution of neurocan distinguishes forming afferent and efferent axonal pathways. J Comp Neurol 355:615-628.
39. Miller PD, Styren SD, Lagenaur CF, DeKosky ST (1994) Embryonic neural cell adhesion molecule (N-CAM) is elevated in the denervated rat dentate gyrus. J Neurosci 14:4217-4225.
40. Nadler JV, Cotman CW, Lynch G (1977) Histochemical evidence of altered development of cholinergic fibers in the rat dentate gyrus following lesions. I. Time course after complete unilateral entorhinal lesion at various ages. J Comp Neurol 171:561-588.
41. Nakic M, Mitrovic N, Sperk G, Schachner M (1996) Kainic acid activates transient expression of tenascin-C in the adult rat hippocampus. J Neurosci Res 44:355-362.
42. Naumann T, Deller T, Bender R, Frotscher M (1997) 192 IgG-saporininduced loss of cholinergic neurons in the septum abolishes cholinergic sprouting after unilateral entorhinal lesion in the rat. Eur J Neurosci 9:1304-1313.
43. 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 rat cerebrum. Neuroscience 60:145-157.
44. Pearlman AL, Sheppard AM (1996) Extracellular matrix in early cortical development. Prog Brain Res 108:117-134.
45. Raisman G (1969) Neuronal plasticity in the septal nuclei of the adult rat. Brain Res 14:25-48.
46. Rauch U (1997) Modeling an extracellular environment for axonal pathfinding and fasciculation in the cerebral nervous system. Cell Tissue Res 290:349-356.
47. 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.
48. 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 271:19536-19547.
49. Rauch U, Clement A, Retzler C, Fröhlich L, Fässler R, Göhring W, Faissner A (1997) Mapping of a defined neurocan binding site to distinct domains of tenascin-C. J Biol Chem 272:26905-26912.
50. Retzler C, Göhring W, Rauch U (1996) Analysis of neurocan structures interacting with the neural cell adhesion molecule N-CAM. J Biol Chem 271:27304-27310.
51. Steward O, Vinsant SL (1983) The process of reinnervation in the dentate gyrus of the adult rat: a quantitative electron microscopic analysis of terminal proliferation and reactive synaptogenesis. J Comp Neurol 214:370-386.
52. Steward O, Torre ER, Phillips L, Trimmer PA (1990) The process of reinnervation in the dentate gyrus of adult rats: time course of increases in mRNA for glial fibrillary acidic protein. J Neurosci 10:2373-2384.
53. Steward O, Kelley MS, Torre ER (1993) The process of reinnervation in the dentate gyrus of adult rats: temporal relationship between changes in the level of glial fibrillary acidic protein (GFAP) and GFAP mRNA in reactive astrocytes. Exp Neurol 124:167-183.
54. Stichel CC, Müller HW (1998) The CNS lesion scar: new vistas on an old regeneration barrier. Cell Tissue Res 294:1-9.
55. Tuttle R, Braisted JE, Richards LJ, O'Leary DD (1998) Retinal axon guidance by region-specific cues in diencephalon. Development 125:791-801.
56. 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.
57. Wyss JM (1981) An autoradiographic study of the efferent connections of the entorhinal cortex in the rat. J Comp Neurol 199:495-512.
58. 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.
59. Yamaguchi Y (1996) Brevican: a major proteoglycan in adult brain. Perspect Dev Neurobiol 3:307-317.