Astroglial ciliary neurotrophic factor mRNA expression is increased in fields of axonal sprouting in deafferented hippocampus

Journal of Comparative Neurology

Volumn 386, Issue 1, 1997, Pages 137-148

  Guthrie, Kathleen M ^a   Woods, Alisa G ^b   Nguyen, Thomas ^a   Gall, Christine M ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Astrocytes; Basic fibroblast growth factor; Ciliary neurotrophic factor; Gliosis; Insulin like growth factor 1; Perforant path

Indexed keywords

CILIARY NEUROTROPHIC FACTOR; MESSENGER RNA;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CONTROLLED STUDY; DEAFFERENTATION; GLIOSIS; HIPPOCAMPUS; MACROGLIA; MALE; NERVE FIBER REGENERATION; NERVE SPROUTING; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT;

AFFERENT PATHWAYS; ANIMALS; ASTROCYTES; AXONS; BRAIN; CILIARY NEUROTROPHIC FACTOR; ENTORHINAL CORTEX; HIPPOCAMPUS; MALE; NERVE GROWTH FACTORS; NERVE REGENERATION; NERVE TISSUE PROTEINS; NEURONAL PLASTICITY; OLFACTORY NERVE; RATS; RATS, SPRAGUE-DAWLEY; RNA, COMPLEMENTARY; RNA, MESSENGER; TRANSCRIPTION, GENETIC;

EID: 0030761044     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19970915)386:1<137::AID-CNE12>3.0.CO;2-H     Document Type: Article

References (73)

1. Amaral, D.G., and M.P. Witter (1995) Hippocampal Formation. The rat nervous system. San Diego: Academic Press, pp. 443-493.
2. Beck, K.D., F. Lamballe, R. Klein, M. Barbacid, P.E. Schauwecker, T.H. McNeill, C.E. Finch, F. Hefti, and J.R. Day (1993) Induction of noncatalytic trkB neurotrophin receptors during axonal sprouting in the adult hippocampus. J. Neurosci. 13:4001-4014.
3. Bizon, J.M., J.C. Lauterborn, P.J. Isackson, and C.M. Gall (1996) Acidic fibroblast growth factor mRNA is expressed by basal forebrain and striatal cholinergic neurons. J. Comp. Neurol. 366:379-389.
4. Bondy, C.A. (1991) Transient IGF-I gene expression during the maturation of functionally related central projection neurons. J. Neurosci. 11:3442-3455.
5. Caroni, P., and P. Grandes (1990) Nerve sprouting in innervated adult skeletal muscle induced by exposure to elevated levels of insulin-like growth factors. J. Cell Biol. 110:1307-1317.
6. Carroll, P., M. Airaksinen, H. Bock, J. Cooper, M. Meyer, E. Pera, M. Sendtner, and H. Thoenen (1995) Expression of CNTF: New perspectives revealed by a lacZ reporter gene introduced into the CNTF gene locus. Soc. Neurosci. Abstr. 21:2011.
7. Conner, J.M., B. Fass-Holmes, and S. Varon (1994) Changes in nerve growth factor immunoreactivity following entorhinal cortex lesions: Possible molecular mechanism regulating cholinergic sprouting. J. Comp. Neurol. 345:409-418.
8. Curtis, R., K.M. Adryan, Y. Zhu, P.J. Harkness, R.M. Lindsay, and P.S. DiStefano (1993) Retrograde axonal transport of ciliary neurotrophic factor is increased by peripheral nerve injury. Nature 365:253-255.
9. Dobrea, G.M., J.R. Unerstall, and M.S. Rao (1992) The expression of CNTF message and immunoreactivity in the central and peripheral nervous system of the rat. Dev. Brain Res. 66:209-219.
10. Fagan, A.M., and F.H. Gage (1990) Cholinergic sprouting in the hippocampus: A proposed role for IL-1. Exp. Neurol. 110:105-120.
11. Fagan, A.M., and F.H. Gage (1994) Mechanisms of sprouting in the adult central nervous system: Cellular responses in areas of terminal degeneration and reinnervation in the rat hippocampus. Neuroscience 58:705-725.
12. Friedman, B., S.S. Scherer, J.S. Rudge, M. Helgren, D. Morrisey, J. McClain, D. Wang, S.J. Wiegand, M.E. Furth, R.M. Lindsay, and N.Y. Ip (1992) Regulation of ciliary neurotrophic factor expression in myelin-related Schwann cells in vivo. Neuron 9:295-305.
13. Gall, C. (1990) Comparative anatomy of the hippocampus: with special reference to differences in the distribution of neuroactive peptides. In E.G. Jones and A. Peters (eds): Cerebral Cortex. New York: Plenum Press, pp. 167-207.
14. Gall, C., and J.C. Lauterborn (1992) Dentate gyrus as a model system for studies of neurotrophic factor regulation in CNS: Seizure studies. In C. Ribak, C. Gall, and I. Mody (eds): The Dentate Gyrus and its Role in Seizures. Amsterdam: Elsevier, pp. 171-185.
15. Gall, C., and G. Lynch (1981) Accelerated rates of synaptogenesis by "sprouting" afferents in the immature hippocampal formation. J. Comp. Neurol. 193:1047-1063.
16. Gall, C., G. Rose, and G. Lynch (1979) Proliferative and migratory activity of glial cells in the partially deafferented hippocampus. J. Comp. Neurol. 183:539-550.
17. Gall, C., G. Ivy, and G. Lynch (1986) Neuroanatomical Plasticity: Its role in organizing and reorganizing the central nervous system. In F. Falkner and J.M. Tanner (eds): Human Growth. New York: Plenum Press, pp. 411-436.
18. Gall, C.M., B. Berschauer, and P.J. Isackson (1994) Basic fibroblast growth factor mRNA is increased in forebrain neurons and glia following recurrent limbic seizures. Mol. Brain Res. 21:190-205.
19. Gall, C., J.C. Lauterborn, and K.M. Guthrie (1995) In Situ Hybridization: A sensitive measure of activity dependent changes in neuronal gene expression. In W.E. Stumpf and H.F. Solomon (eds): In Vitro/In Vivo Autoradiography and Correlative Imaging. New York: Academic Press, pp. 379-399.
20. Gehrmann, J., S.W. Schoen, and G.W. Kreutzberg (1991) Lesion of rat entorhinal cortex leads to a rapid microglial reaction in the dentate gyrus: A light and electron microscopical study. Acta Neuropathol. 82:442-455.
21. Glazner, G.W., A.E. Morrison, and D.N. Ishii (1994) Elevated insulin-like growth factor (IGF) gene expression in sciatic nerves during IGF-supported nerve regeneration. Mol. Brain Res. 25:265-272.
22. Goldowitz, D., and C.W. Cotman (1980) Do neurotrophic interactions control synapse formation in the adult rat brain? Brain Res. 181:325-344.
23. Goldowitz, D., W.F. White, O. Steward, G. Lynch, and C. Cotman (1975) Anatomical evidence for a projection from the entorhinal cortex to the contralateral dentate gyrus of the rat. Exp. Neurol. 47:433-441.
24. Gómez-Pinilla, F., J.W.-K. Lee, and C.W. Cotman (1992) Basic FGF in adult rat brain: Cellular distribution and response to entorhinal lesion and fimbria-fornix transection. J. Neurosci. 12:345-355.
25. Guilian, D., and L. Lachman (1985) Interleukin-1 stimulation of astroglial proliferation after brain injury. Science 228:497-499.
26. Gurney, M.E., H. Yamamoto, and Y. Kwon (1992) Induction of motor neuron sprouting in vivo by ciliary neurotrophic factor and basic fibroblast growth factor. J. Neurosci. 12:3241-3247.
27. Guthrie, K.M., T. Nguyen, and C.M. Gall (1995) Insulin-like growth factor-1 mRNA is increased in deafferented hippocampus: Spatiotemporal correspondence of a trophic event with axon sprouting. J. Comp. Neurol. 352:147-160.
28. Hagg, T., D. Quon, J. Higaki, and S. Varon (1992) Ciliary neurotrophic factor prevents neuronal degeneration and promotes low affinity NGF receptor expression in the adult CNS. Neuron 8:145-158.
29. Hagg, T., S. Varon, and J. Louis (1993) Ciliary neurotrophic factor (CNTF) promotes low-affinity nerve growth factor receptor and CD4 expression by rat CNS microglia. J. Neuroimmunol. 48:177-188.
30. Han, V.K.M., J.M. Lauder, and A.J. D'Ercole (1987) Characterization of somatomedin/insulin-like growth factor receptors and correlations with biologic actions in cultured neonatal rat astroglial cells. J. Neurosci. 7:501-511.
31. Han, V.K.M., A. Smith, W. Myint, K. Nygard, and S. Bradshaw (1992) Mitogenic activity of epidermal growth factor on newborn rat astroglia: Interaction with insulin-like growth factors. Endocrinology 131:1134-1142.
32. Heumann, R., S. Korsching, C. Bandtlow, and H. Thoenen (1987) Changes of nerve growth factor synthesis in nonneuronal cells in response to sciatic nerve transection. J. Cell Biol. 104:1623-1631.
33. Hjörth-Simonsen, A. (1972) Projection of the lateral part of the entorhinal area to the hippocampus and fascia dentata. J. Comp. Neurol. 146:219-232.
34. Hudson, L.D., J.A. Berndt, C. Puckett, C.A. Kozak, and R.A. Lazzarini (1987) Aberrant splicing of proteolipid protein mRNA in the dysmyelinating jimpy mutant mouse. Proc. Natl. Acad. Sci. USA 84:1454-1458.
35. Ip, N.Y., J. McClain, N.X. Barrezueta, T.H. Aldrich, L. Pan, Y. Li, S.J. Wiegand, B. Friedman, S. Davis, and G.D. Yancopoulos (1993a) The a component of the CNTF receptor is required for signaling and defines potential CNTF targets in the adult and during development. Neuron 10:89-102.
36. Ip, N.Y., S.J. Wiegand, J. Morse, and J.S. Rudge (1993b) Injury-induced regulation of ciliary neurotrophic factor mRNA in adult rat brain. Eur. J Neurosci. 5:25-33.
37. Ishii, D.N., G.W. Glazner, and S.F. Pu (1994) Role of insulin-like growth factors in peripheral nerve regeneration. Pharmacol. Ther. 62:125-144.
38. Jensen, M.B., B. Gonzalez, B. Castelano, and J. Zimmer (1994) Microglial and astroglial reactions to anterograde axonal degeneration: A histochemical and immunocytochemical study of the adult rat fascia dentata after entorhinal perforant path lesions. Exp. Brain Res. 98:245-260.
39. Johnson, E.M., M. Taniuchi, and P.S. DiStefano (1988) Expression and possible function of nerve growth factor receptors on Schwann cells. TINS 11:299-304.
40. Kanje, M., A. Skottner, J. Sjoberg, and G. Lundborg (1989) Insulin-like growth factor 1 (IGF-1) stimulates regeneration of the rat sciatic nerve. Brain Res. 486:396-398.
41. Kato, A.C., and R.M. Lindsay (1994) Overlapping and additive effects of neurotrophins and CNTF on cultured human spinal cord neurons. Exp. Neurol. 130:196-201.
42. Kwon, Y.W., and M.E. Gurney (1994) Systemic injections of ciliary neurotrophic factor induce sprouting by adult motor neurons. Neuroreport 5:789-792.
43. Lapchak, P.A., D.M. Araujo, K.D. Beck, C.E. Finch, S.A. Johnson, and F. Hefti (1993) BDNF and trkB mRNA expression in the hippocampal formation of aging rats. Neurobiol. Aging 14:121-126.
44. Laquierriere, A., P. Peulve, O. Jin, J. Tiollier, M. Tardy, H. Vaudry, J. Hemet, and M. Tadie (1994) Effect of basic fibroblast growth factor and a-melanocyte stimulating hormone on nerve regeneration through a collagen channel. Microsurgery 15:203-210.
45. Lee, K., E. Stanford, C. Cotman, and G. Lynch (1977) Ultrastructural evidence for bouton proliferation in the partially deafferented dentate gyrus of the adult rat. Exp. Brain Res. 29:475-485.
46. Lee, M., T. Deller, M. Kirsch, M. Frotscher, and H. Hofman (1997) Differential regulation of ciliary neurotrophic factor (CNTF) and CNTF receptor-α expression in astrocytes and neurons of the fascia dentata after entorhinal cortex lesion. J. Neurosci. 17:1137-1146.
47. Levinson, S.W., M.H. Duccheschi, G.M. Young, and T.L. Wood (1996) Acute exposure to CNTF in vivo induces multiple components of reactive gliosis. Exp. Neurol. 141:256-268.
48. Liesi, P., S. Kaakkola, D. Dahl, and A. Vaheri (1984) Laminin is induced in astrocytes of adult brain by injury. EMBO J. 3:683-686.
49. Lynch, G., G. Rose, C. Gall, and C.W. Cotman (1975) The response of the dentate gyrus to partial deafferentation. In M. Santini (ed): Golgi Centennial Symposium Proceedings. New York: Raven Press, pp. 305-317.
50. Lynch, G., C. Gall, and C. Cotman (1977) Temporal parameters of axon sprouting in the adult brain. Exp. Neurol. 54:179-183.
51. Matthews, D.A., C. Cotman, and G. Lynch (1976) 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.
52. Mitsumoto, H., K. Ikeda, B. Klinkosz, J.M. Cedarbaum, V. Wong, and R.M. Lindsay (1994) Arrest of motor neuron disease in wobbler mice cotreated with CNTF and BDNF. Science 265:1107-1110.
53. Miyagawa, T., H. Saito, and N. Nishiyama (1993) Branching enhancement by basic fibroblast growth factor in cut neurite of hippocampal neurons. Neurosci. Lett. 153:29-31.
54. Miyamoto, O., T. Itano, M. Fujisawa, M. Tokuda, H. Matsui, S. Magao, and O. Hatase (1993) Exogenous basic fibroblast growth factor and nerve growth factor enhance sprouting of acetylcholinesterase positive fibers in denervated rat hippocampus. Acta. Med. Okayama 47:139-144.
55. Motulsky, H. (1995) Intuitive Biostatistics. New York: Oxford University Press.
56. Perraud, F., F. Besnard, B. Pettmann, M. Sensenbrenner, and G. Labourdette (1988) Effects of acidic and basic fibroblast growth factors (aFGF and bFGF) on the proliferation and the glutamine synthetase expression of rat astroblasts in culture. Glia 1:124-131.
57. Pico, R.M., and C.M. Gall (1994) Hippocampal epileptogenesis produced by electrolytic iron deposition in the rat dentate gyrus. Epilepsy Res. 19:27-36.
58. Rivera, S., S. Gold, and C.M. Gall (1994) Interleukin-1β increases basic fibroblast growth factor mRNA expression in adult rat brain and organotypic hippocampal cultures. Mol. Brain Res. 27:12-26.
59. Rudge, J.S., R.F. Alderson, E. Pasnilowski, J. McClain, N.Y. Ip, and R.M. Lindsay (1992) Expression of ciliary neurotrophic factor and the neurotrophins - nerve growth factor, brain-derived neurotrophic factor and neurotrophin-3 - in cultured rat hippocampal astrocytes. Eur. J. Neurosci. 4:459-471.
60. Rudge, J.S., Y. Li, E. Pasnikowski, K. Mattson, L. Pan, G.D. Yancopoulos, S.J. Wiegand, R.M. Lindsay, and N.Y. Ip (1994) Neurotrophic factor receptors and their signal transduction capabilities in rat astrocytes. Eur. J. Neurosci. 6:693-705.
61. Sahenk, Z., J. Seharaseyon, and J.R. Mendell (1994) CNTF potentiates peripheral nerve regeneration. Brain Res. 655:246-250.
62. Sendtner, M., K.A. Stockli, and H. Thoenen (1992) Synthesis and localization of ciliary neurotrophic factor in the sciatic nerve of the adult rat after lesion and during regeneration. J. Cell Biol. 118:139-148.
63. Shimatsu, A., and P. Rotwein (1987) Sequence of two rat insulin-like growth factor I mRNAs differing within the 5′ untranslated region. Nucleic Acids Res. 15:7196.
64. Shiota, C., M. Miura, and K. Mikoshiba (1989) Developmental profile and differential localization of mRNAs of myelin basic proteins (MBP and PLP) in oligodendrocytes in the brain and in culture. Dev. Brain Res. 45:83-94.
65. Steward, O., and S.L. Vinsant (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.
66. Stöckli, K.A., F. Lottspeich, M. Sendtner, P. Masiakowski, P. Carroll, R. Gotz, D. Lindholm, and H. Thoenen (1989) Molecular cloning, expression and regional distribution of rat ciliary neurotrophic factor. Nature 342:920-923.
67. Stöckli, K.A., L.E. Lillien, M. Näher-Noé, G. Brietfield, R.A. Hughes, H. Thoenen, and M. Sendtner (1991) Regional distribution, developmental changes and cellular localization of CNTF-mRNA and protein in the rat brain. J. Cell Biol. 115:447-459.
68. Streit, W., and G. Kreutzberg (1987) Lectin binding by resting and reactive microglia. J. Neurocytol. 16:249-260.
69. Tuszynski, M.H., and F.H. Gage (1995) Maintaining the neuronal phenotype after injury in the adult CNS: Neurotrophic factors, axonal growth substrates and gene therapy. Mol. Neurobiol. 10:151-166.
70. Van Der Zee, C.E.E.M., J. Fawcett, and J. Diamond (1992) Antibody to NGF inhibits collateral sprouting of septohippocampal fibers following entorhinal cortex lesion in adult rats. J. Comp. Neurol. 326:91-100.
71. Winter, C.G., Y. Saotome, S.W. Levinson, and D. Hirsh (1995) A role for ciliary neurotrophic factor as an inducer of reactive gliosis, the glial response to central nervous system injury. Proc. Natl. Acad. Sci. USA 92:5865-5869.
72. Yoshida, K., and F.H. Gage (1991) Fibroblast growth factors stimulate nerve growth factor synthesis and secretion by astrocytes. Brain Res. 538:118-126.
73. Zimmer, J. (1973) Extended commissural and ipsilateral projections in postnatally deentorhinated hippocampus and fascia dentata demonstrated in rats by silver impregnation. Brain Res. 64:293-311.