Up-regulation of astrocyte-derived tenascin-C correlates with neurite outgrowth in the rat dentate gyrus after unilateral entorhinal cortex lesion

Neuroscience

Volumn 81, Issue 3, 1997, Pages 829-846

  Deller, T ^a   Haas, C A ^a   Naumann, T ^a   Joester, A ^b   Faissner, A ^b   Frotscher, M ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

^b UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

Astroglia; Axon growth; Extracellular matrix; Phagocytosis; Plasticity; Sprouting

Indexed keywords

TENASCIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; DENERVATION; DENTATE GYRUS; ELECTRON MICROSCOPY; ENTORHINAL CORTEX; EXTRACELLULAR MATRIX; IMMUNOCOMPETENT CELL; IMMUNOHISTOCHEMISTRY; NERVE FIBER GROWTH; NONHUMAN; PRIORITY JOURNAL; RAT; RECEPTOR UPREGULATION;

ANIMALS; ASTROCYTES; AXONS; DENTATE GYRUS; ENTORHINAL CORTEX; FEMALE; IMMUNOHISTOCHEMISTRY; MALE; NERVE DEGENERATION; NERVE ENDINGS; NEURITES; PHAGOCYTOSIS; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER; TENASCIN;

EID: 0031587280     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(97)00194-2     Document Type: Article

References (95)

1. Amaral D., and Witter M. P. (1995) The hippocampal formation. In The Rat Nervous System, 2nd edn (ed. Paxinos G.), pp. 443-494. Academic Press, San Diego.
2. Bartsch S., Bartsch U., Dorries U., Faissner A., Weller A., Ekblom P., Schachner M. Expression of tenascin in the developing and adult cerebellar cortex. J. Neurosci. 12:1992;736-749.
3. Ben-Ari Y. Limbic seizure and brain damage produced by kainic acid: mechanisms and relevance to human temporal lobe epilepsy. Neuroscience. 14:1985;375-403.
4. Benowitz L. I., Rodriguez W. R., Neve R. L. The pattern of GAP-43 immunostaining changes in the rat hippocampal formation during reactive synaptogenesis. Molec. Brain Res. 8:1990;17-23.
5. Conner J. M., Fass-Holmes B., Varon S. Changes in nerve growth factor immunoreactivity following entorhinal cortex lesions: possible molecular mechanism regulating cholinergic sprouting. J. comp. Neurol. 345:1994;409-418.
6. Cotman C. W., and Nadler J. V. (1978) Reactive synaptogenesis in the hippocampus. In Neuronal Plasticity (ed. Cotman C. W.), pp. 227-271. Raven Press, New York.
7. Cotman C. W., Nieto-Sampedro M., Harris E. W. Synapse replacement in the nervous system of adult vertebrates. Physiol. Rev. 61:1981;684-784.
8. Day J. R., Laping N. J., Lampert-Etchells M., Brown S. A., O'Callaghan J. P., McNeill T. H., Finch C. E. Gonadal steroids regulate the expression of glial fibrillary acidic protein in the adult male rat hippocampus. Neuroscience. 55:1993;435-443.
9. Day J. R., Laping N. J., McNeill T. H., Schreiber S. S., Pasinetti G., Finch C. E. Castration enhances expression of glial fibrillary acidic protein and sulfated glycoprotein-2 in the intact and lesion-altered hippocampus in the adult male rat. Molec. Endocr. 4:1990;1995-2002.
10. Deller T., Frotscher M., Nitsch R. 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. 15:1995;6868-6878.
11. Deller T., Frotscher M., Nitsch R. Sprouting of crossed entorhino-dentate fibers after a unilateral entorhinal lesion: anterograde tracing of fiber reorganization with Phaseolus vulgaris-leucoagglutinin (PHAL). J. comp. Neurol. 365:1996;42-55.
12. Deller T., Martinez A., Nitsch R., Frotscher M. A novel entorhinal projection to the rat dentate gyrus: Direct innervation of proximal dendrites and granule cell bodies of granule cells and GABAergic neurons. J. Neurosci. 16:1996;3322-3333.
13. Deller T., Nitsch R., Frotscher M. Phaseolus vulgaris leucoagglutinin (PHAL) tracing of commissural fibers to the rat dentate gyrus: evidence for a previously unknown commissural projection to the outer molecular layer. J. comp. Neurol. 352:1995;55-68.
14. Deller T., Nitsch R., Frotscher M. Layer-specific sprouting of commissural fibers to the rat fascia dentate after unilateral entorhinal cortex lesion: A Phaseolus vulgaris leucogglutinin tracing study. Neuroscience. 71:1996;651-660.
15. Erickson H. P. Tenascin-C, tenascin-R and tenascin-X: a family of talented proteins in search of functions. Curr. Opin. Cell Biol. 5:1993;869-876.
16. Fagan A. M., Gage F. H. Cholinergic sprouting in the hippocampus: a proposed role for IL-I. Expl Neurol. 110:1990;105-120.
17. Faissner A. (1996) The tenascin gene family in development and plasticity of neural tissues. In Tenascin and Counteradhesive Molecules of the Extracellular Matrix (ed. Crossin K. L.), pp. 47-87. Harwood Academic Publishers, Buffalo.
18. Faissner A., Clement A., Lochter A., Streit A., Mandl C., Schachner M. Isolation of a neural chondroitin sulfate proteoglycan with neurite outgrowth promoting properties. J. Cell Biol. 126:1994;783-799.
19. Faissner A., Götz B., Joester A., Scholze A. The tenascin gene family-versatile glycoproteins implicated in neural pattern formation and regeneration. Semin. dev. Biol. 6:1995;139-148.
20. Faissner A., Kruse J. J1/tenascin is a repulsive substrate for central nervous system neurons. Neuron. 5:1990;627-637.
21. Faissner A., Scholze A., Götz B. Tenascin glycoproteins in developing neural tissues - only decoration? Persp. dev. Neurobiol. 2:1994;53-66.
22. Faissner A., Steindler D. Boundaries and inhibitory molecules in developing neural tissues. Glia. 13:1995;233-254.
23. Ferhat L., Chevassus Au Louis N., Jorquera I., Niquet J., Khrestchatisky M., Ben-Ari Y., Represa A. Transient increase of tenascin-C in immature hippocampus: astroglial and neuronal expression. J. Neurocytol. 25:1996;53-66.
24. Frotscher M., Heimrich B., Deller T. Sprouting in the hippocampus is layer specific. Trends Neurosci. 20:1997;218-223.
25. Gage F. H., Olejniczak P., Armstrong D. M. Astrocytes are important for sprouting in the septohippocampal circuit. Expl Neurol. 102:1988;2-13.
26. Gehrmann J., Schön S. W., Kreutzberg G. W. Lesion of the rat entorhinal cortex leads to a rapid microglial reaction in the dentate gyrus. Acta neuropath. 82:1991;442-455.
27. Godfraind C., Schachner M., Goffinet A. M. Immunohistochemical localisation of cell adhesion molecules L1, J1, N-CAM and their common carbohydrate L2 in the embryonic cortex of normal and reeler mice. Brain Res. 470:1988;99-111.
28. Goldowitz D., Cotman C. W. Axonal transport and axon sprouting in the adult rat dentate gyrus: an autoradiographic study. Neuroscience. 5:1980;2163-2174.
29. Goldowitz D., White W. F., Steward O., Cotman C. W., Lynch G. Anatomical evidence for a projection from the entorhinal cortex to the contralateral dentate gyrus of the rat. Expl Neurol. 47:1975;433-441.
30. Gomez-Pinilla F., Lee J. W., Cotman C. W. Basic FGF in adult rat brain: cellular distribution and response to entorhinal lesion and fimbria-fornix transection. J. Neurosci. 12:1992;345-355.
31. Götz B., Scholze A., Clement A., Joester A., Schütte K., Wigger F., Frank R., Spiess E., Ekblom P., Faissner A. Tenascin-C contains distinct adhesive, anti-adhesive, and neurite outgrowth promoting sites for neurons. J. Cell Biol. 132:1996;681-699.
32. Gwag B. J., Sessler F., Kimmerer K., Springer J. E. Neurotrophic factor mRNA expression in the dentate gyrus is increased following angular bundle transection. Brain Res. 647:1994;23-29.
33. Hoff S. F., Scheff S. W., Bernardo L. S., Cotman C. W. Lesion-induced synaptogenesis in the dentate gyrus of aged rats. I. Loss and recquisition of normal synaptic density. J. comp. Neurol. 205:1982;246-252.
34. Hoff S. F., Scheff S. W., Cotman C. W. Lesion-induced synaptogenesis in the dentate gyrus of aged rats. II. Demonstration of an impaired degeneration clearing response. J. comp. Neurol. 205:1982;253-259.
35. Husmann K., Faissner A., Schachner M. Tenascin promotes cerebellar granule cell migration and neurite outgrowth by different domains in the fibronectin type III repeats. J. Cell Biol. 116:1992;1475-1486.
36. Jucker M., D'Amato F., Mondadori C., Mohajeri H., Magyar J., Bartsch U., Schachner M. Expression of the neural adhesion molecule Ll in the deafferented dentate gyrus. Neuroscience. 75:1996;703-715.
37. Jucker M., Mondadori C., Mohajeri H., Bartsch U., Schachner M. Transient upregulation of N-CAM mRNA in astrocytes in response to entorhinal cortex lesions and ischemia. Molec. Brain Res. 28:1995;149-156.
38. 125I]insulin receptor binding sites in the rat hippocampal formation. Neuroscience. 55:1993;69-80.
39. Kelly M. S., Steward O. The role of postlesion seizures and spreading depression in the upregulation of glial fibrillary acidic protein mRNA after entorhinal cortex lesions. Expl Neurol. 139:1996;83-94.
40. Kruse J., Keilhauer G., Faissner A., Timpl R., Schachner M. The J1 glycoprotein - a novel nervous system cell adhesion molecule of the L2/HNK-1 family. Nature. 227:1985;680-685.
41. Langenfeld-Oster B., Faissner A., Irintchev A., Wernig A. Polyclonal antibodies against N-CAM and tenascin delay endplate reinnervation. J. Neurocytol. 23:1994;591-604.
42. Laywell E. D., Dörries U., Bartsch U., Faissner A., Schachner M., Steindler D. A. Enhanced expression of the developmentally regulated extracellular matrix molecule tenascin following adult brain injury. Proc. natn. Acad. Sci. U.S.A. 89:1992;2634-2638.
43. Lee K. S., Stanford E. J., Cotman C. W., Lynch G. S. Ultrastructural evidence for bouton proliferation in the partially deafferented dentate gyrus of the adult rat. Expl Brain Res. 29:1977;475-485.
44. Lee W. H., Michels K. M., Bondy C. A. Localization of insulin-like growth factor binding protein-2 messenger RNA during postnatal brain development: correlation with insulin-like growth factors I and II. Neuroscience. 53:1993;251-265.
45. Lin L.-H., Bock S., Carpenter K., Rose M., Norden J. J. Synthesis and transport of GAP-43 in entorhinal cortex neurons and perforant pathway during lesion-induced sprouting and reactive synaptogenesis. Molec. Brain Res. 14:1992;147-153.
46. Lochter A., Vaughan L., Kaplony A., Prochiantz A., Schachner M., Faissner A. J1/tenascin in substrate-bound and soluble form displays contrary effects on neurite outgrowth. J. Cell Biol. 113:1991;1159-1171.
47. Lynch G. and Cotman C. W. (1975) The hippocampus as a model for studying anatomical plasticity in the adult brain. In The Hippocampus, Vol. 1 (eds Isaacson R. L. and Pribram K. H.) pp. 123-154. Plenum Press, New York.
48. Lynch G., Gall C., Rose G., Cotman C. W. Changes in the distribution of the dentate gyrus associational system following unilateral or bilateral entorhinal lesion in the adult rat. Brain Res. 110:1976;57-71.
49. Lynch G., Matthews D. A., Mosko S., Parks T., Cotman C. W. Induced acetylcholinesterase-rich layer in rat dentate gyrus following entorhinal lesions. Brain Res. 42:1972;311-318.
50. Lynch G., McWilliam R., Gall C. The effects of successive lesions on the time course of the sprouting response in the hippocampus of the rat. Brain Res. 240:1982;154-157.
51. Lynch G., Stanfield B., Cotman C. W. Developmental differences in postlesion axonal growth in the hippocampus. Brain Res. 59:1973;155-168.
52. Masliah E., Fagan A. M., Terry R. D., DeTeresa R., Mallory M., Gage F. H. Reactive synaptogenesis assessed by synaptophysin immunoreactivity is associated with GAP-43 in the dentate gyrus of the adult rat. Expl Neurol. 113:1991;131-142.
53. Matthews D. A., Cotman C. W., Lynch G. 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. 115:1976;1-21.
54. Matthews D. A., Cotman C. W., Lynch G. 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. 115:1976;23-41.
55. Mège R. M., Nicolet M., Pincon-Rymond M., Murawsky M., Rieger F. Cytotactin is involved in synaptogenesis during regeneration of the frog neuromuscular system. Devl Biol. 149:1992;381-394.
56. Mesulam M.-M., Geula C., Moran M. A. Anatomy of cholinesterase inhibition in Alzheimer's disease: Effect of physostigmine and tetrahydroaminoacridine on plaques and tangles. Ann. Neurol. 22:1987;683-691.
57. Miller P. D., Styren S. D., Lagenaur C. F., DeKosky S. T. Embryonic neural cell adhesion molecule (N-CAM) is elevated in the denervated rat dentate gyrus. J. Neurosci. 14:1994;4217-4225.
58. Mitrovic N., Dorries U., Schachner M. Expression of the extracellular matrix glycoprotein tenascin in the somatosensory cortex of the mouse during postnatal development: an immunocytochemical and in situ hybridisation analysis. J. Neurocytol. 23:1994;264-378.
59. Morgan T. E., Nichols N. R., Pasinetti G. M., Finch C. E. TGF-β1 mRNA increases in macrophage/microglial cells of the hippocampus in response to deafferentation and kainic acid-induced neurodegeneration. Expl Neurol. 120:1993;291-301.
60. Nadler J. V., Cotman C. W., Lynch G. 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. 171:1977;561-588.
61. Nakic M., Mitrovic N., Sperk G., Schachner M. Kainic acid activates transient expression of tenascin-C in the adult rat hippocampus. J. Neurosci. Res. 44:1996;355-362.
62. Nieto-Sampedro M., Bovolenta P. Growth factors and growth factor receptors in the hippocampus. Role in plasticity and response to injury. Prog. Brain Res. 83:1990;341-355.
63. Niquet J., Jorquera I., Faissner A., Ben-Ari Y., Represa A. Gliosis and axonal sprouting in the hippocampus of epileptic rats are associated with an increase of tenascin-C immunoreactivity. J. Neurocytol. 24:1995;611-624.
64. Norris J. G., Benveniste E. N. Interleukin-6 production by astrocytes: induction by the neurotransmitter norepinephrine. J. Neuroimmunol. 45:1993;137-145.
65. Nyakas C., Luiten P. G. M., Balkan B., Spencer D. G. Jr. Changes in septohippocampal projections after lateral entorhinal or combined entorhinal-raphe lesions as studied by anterograde tracing methods. Brain Res. Bull. 21:1988;285-293.
66. Paxinos G. and Watson C. (1986) Atlas of the Rat Brain in Stereotaxic Coordinates. Academic Press, San Diego.
67. Pechan P. A., Chowdhury K., Gerdes W., Seifert W. Glutamate induces the growth factors NGF, bFGF, the receptor FGF-R1 and c-fos mRNA expression in rat astrocytic culture. Neurosci. Lett. 153:1993;111-114.
68. Rose G., Lynch G., Cotman C. W. Hypertrophy and redistribution of astrocytes in the deafferented dentate gyrus. Brain Res. Bull. 1:1976;87-92.
69. Schauwecker P. E., Cheng H.-W., Serquinia R. M. P., Mori N., McNeill T. H. Lesion-induced sprouting of commissural/associational axons and induction of GAP-43 mRNA in hilar and CA3 pyramidal neurons in the hippocampus are diminished in aged rats. J. Neurosci. 15:1995;2462-2470.
70. Scheff S. W., DeKosky S. T. Glucocorticoid suppression of lesion-induced synaptogenesis: effect of temporal manipulation of steroid treatment. Expl Neurol. 105:1989;260-264.
71. Scheffler B., Faissner A., Beck H., Behle K., Wolf H. K., Wiestler O. D., Blumcke I. Hippocampal loss of tenascin boundaries in Ammon's horn sclerosis. Glia. 19:1997;35-96.
72. Schön S. W., Kreutzberg G. W. Synaptic 5′-nucleotidase activity reflects lesion-induced sprouting within the adult rat dentate gyrus. Expl Neurol. 127:1994;106-118.
73. Schwartz J. P., Nishiyama N. Neurotrophic factor gene expression in astrocytes during development and following injury. Brain Res. Bull. 35:1994;403-407.
74. Springer J. E., Gwag B. J., Sessler F. M. Neurotrophic factor mRNA expression in dentate gyrus is increased following in vivo stimulation of the angular bundle. Molec. Brain Res. 23:1994;135-143.
75. Steindler D. A., Cooper N. G. F., Faissner A., Schachner M. Boundaries defined by adhesion molecules during development of the cerebral cortex: the J1/tenascin glycoprotein in the mouse somatosensory cortical barrel field. Devl Biol. 131:1989;243-260.
76. Stern C. D., Norris W. E., Bronner-Fraser M., Carlson G. J., Faissner A., Keynes R. J., Schachner M. J1/tenascin-related molecules are not responsible for the segmented pattern of neural crest cells or motor axons in the chick embryo. Development. 107:1989;309-319.
77. Steward O. Reinnervation of the dentate gyrus by homologous afferents following entorhinal cortex lesion in adult rats. Science. 194:1976;426-428.
78. Steward O. (1986) Lesion-induced synapse growth in the hippocampus: In search of cellular and molecular mechanisms. In The Hippocampus (eds Isaacson R. L. and Pribam K. H.), pp. 65-111. Plenum Press, New York.
79. Steward O. Synapse replacement on cortical neurons following denervation. Cerebral Cortex. 9:1991;81-132.
80. Steward O. Signals that induce sprouting in the central nervous system: sprouting is delayed in a strain of mouse exhibiting delayed axonal degeneration. Expl Neurol. 118:1992;340-351.
81. Steward O. (1994) Reorganization of neuronal circuitry following central nervous system trauma: naturally occurring processes and opportunities for therapeutic intervention. In The Neurobiology of Central Nervous System Trauma (eds Salzman S. K. and Faden A. I.), pp. 266-287. Oxford University Press, New York.
82. Steward O., Cotman C. W., Lynch G. Growth of a new fiber projection in the brain of adult rats: reinnervation of the dentate gyrus by the contralateral entorhinal cortex following ipsilateral entorhinal lesion. Expl Brain Res. 20:1974;45-66.
83. Steward O., Cotman C. W., Lynch G. S. A quantitative autoradiographic and electrophysiological study of the reinnervation of the dentate gyrus by the contralateral entorhinal cortex following ipsilateral entorhinal lesions. Brain Res. 114:1976;181-200.
84. Steward O., Kelly M. S., Torre E. R. The process of reinnervation in the dentate gyrus of adult rats: temporal relationship between changes in the levels of glial fibrillary acidic protein (GFAP) and GFAP mRNA in reactive astrocytes. Expl Neurol. 124:1993;167-183.
85. Steward O., Torre E. R., Phillips L. L., Trimmer P. A. The process of reinnervation in the dentate gyrus of adult rats: time course of increases in mRNA for glial fibriallary acidic protein. J. Neurosci. 10:1990;2373-2384.
86. Steward O., Torre E. R., Tomasulo R., Lothman E. Neuronal activity up-regulates astroglial gene expression. Proc. natn. Acad. Sci. U.S.A. 88:1991;6819-6823.
87. Steward O., Vinsant S. L. 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. 214:1983;370-386.
88. Styren S. D., Lagenaur C. F., Miller P. D., DeKosky S. T. Rapid expression and transport of embryonic N-CAM in dentate gyrus following entorhinal cortex lesion: ultrastructural analysis. J. comp. Neurol. 349:1994;486-492.
89. Styren S. D., Miller P. D., Lagenaur C. F., DeKosky S. T. Alternate strategies in lesion-induced reactive synaptogenesis: differential expression of L1 in two populations of sprouting axons. Expl Neurol. 131:1995;165-173.
90. Trout J. J., Lu C. Y., Goldstone A. D., Sahgal S. Polyamines and NMDA receptors modulate pericapillary astrocyte swelling following cerebral cryo-injury in the rat. J. Neurocytol. 24:1995;341-346.
91. West J. R. Age-dependent sprouting in the dentate gyrus demonstrated with anterograde HRP. Brain Res. Bull. 12:1984;323-330.
92. West J. R., Deadwyler S., Cotman W. M., Lynch G. Time-dependent changes in commissural field potentials in the dentate gyrus following lesions of the entorhinal cortex in adult rats. Brain Res. 97:1975;215-233.
93. Wyss J. M. An autoradiographic study of the efferent connections of the entorhinal cortex in the rat. J. comp. Neurol. 199:1981;495-512.
94. Zhang Y., Anderson P. N., Campbell G., Mohajeri H., Schachner M., Liebermann A. R. Tenascin-C expression by neurons and glial cells in the rat spinal cord: changes during postnatal development and after dorsal root or sciatic nerve injury. J. Neurocytol. 24:1995;585-601.
95. Zimmer J. Extended commissural and ipsilateral projections in postnatally deentorhinated hippocampus and fascia dentata demonstrated in rats by silver impregnation. Brain Res. 64:1973;293-311.