Skip to main content
SpringerLink
Log in

Trophic Control of Central Cholinergic Neuron Development In Vitro

  • Chapter
Brain Repair

Part of the book series: Wenner-Gren Center International Symposium Series ((WGS))

  • 12 Accesses

Abstract

The known role of nerve growth factor (NGF) in the function of the peripheral nervous system supports the concept that neuron-target interactions essential for a given neuron or neural connection to survive during development are based on the production and release of specific trophic molecules by the target area and their action on the innervating neurons (Thoenen and Edgar, 1985; Purves, 1986). Findings obtained during the past decade suggest that NGF plays such a role also in the central nervous system. Actions of NGF on the cholinergic neurons of the basal forebrain and the corpus striatum are well characterized and distribution and developmental changes of NGF and its receptor in the CNS have been extensively investigated (reviews: Thoenen et al., 1987; Whittemore and Seiger, 1987; Hefti et al., 1989). The data are compatible with the view that NGF serves as a target derived survival factor for basal forebrain neurons. However, it is still not known, whether there is neural cell death during development of the basal forebrain or striatal cholinergic system and whether the availability of NGF indeed regulates the number of cholinergic neurons. Furthermore, the selectivity of the action of NGF in the central nervous system remains one of the principal unresolved questions. While the distribution of NGF and its receptor suggest actions of NGF on neurons other than the cholinergic ones (Buck et al., 1988; Ernfors et al., 1988; Schatteman et al., 1988; Yan and Johnson, 1988; Large et al., 1989), no other NGF-responsive central populations nave been identified with certainty yet.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Aizenman, Y., and DeVellis, J. (1987). Brain neurons develop in a serum and glial free environment: effects of transferrin, insulin, insulin-like growth factor-I and thyroid hormone on neuronal survival, growth and differentiation. Brain Res. 406, 32–42.

    Article  PubMed  CAS  Google Scholar 

  • Anderson, K.J., Dam, D., Lee, S., and Cotman, C.W. (1988). Basic fibroblast growth factor prevents death of lesioned cholinergic neurons in vivo. Nature 332, 360–362.

    Article  PubMed  CAS  Google Scholar 

  • Barde, Y-A., Davies, A., M., Johnson, J.,E., Lindsay, R., M., and Thoenen, H. (1987). Brain-derived neurotrophic factor. Prog. Brain. Res. 71, 185–189.

    Article  PubMed  CAS  Google Scholar 

  • Baskin, D.G., Wilcox, B.J., Figlewicz, D.P., and Dorsa, D.M. (1988). Insulin and insulin-like growth factors in the CNS. Trends Neurosci. 11, 107–111.

    Article  PubMed  CAS  Google Scholar 

  • Bassas, L., De Pablo, F., Lesniak, M.A., and Roth, J. (1985). Ontogeny of receptors for insulin-like peptide in chick embryo tissues: Early dominance of insulin-like growth factor over insulin receptors in brain. Endocrinology 117, 2321–2329.

    Article  PubMed  CAS  Google Scholar 

  • Bhat, N. (1983). Insulin dependent neurite outgrowth in cultured embryonic mouse brain cells. Dev. Brain Res. 11, 315–318.

    Article  CAS  Google Scholar 

  • Bohannon, N.J., Corp, E.S., Wilcox, B.J., Figlewicz, D.P., Dorsa, D.M., and Baskin, D.G. (1988). Localization of binding sites for insulin-like growth factor I (IGF-I) in the rat brain by quantitative autoradiography. Brain Res. 444, 205–213.

    Article  PubMed  CAS  Google Scholar 

  • Bothwell, M. (1982). Insulin and somatemedin MSA promote nerve growth factor-independent neurite formation by cultured chick dorsal root ganglionic sensory neurons. J. Neurosci. Res. 8, 225–231.

    Article  PubMed  CAS  Google Scholar 

  • Buck, C.R., Martinez, H.J., Chao, M.V., and Black, I. (1988). Differential expression of the nerve growth factor receptor gene in multiple brain areas. Dev. Brain Res. 44, 259–268.

    Article  CAS  Google Scholar 

  • Burgess, S.K., Jacobs, S., Cuatrecasas, P., and Sahyoun, N. (1987). Characterization of a neuronal subtype of insulin-like growth factor I receptor. J. Biol. Chem. 262, 1618–1622.

    PubMed  CAS  Google Scholar 

  • DiCicco-Bloom, E., and Black, I. (1988). Insulin growth factors regulate the mitotic cycle in cultured rat sympathetic neuroblasts. Proc. Natl. Acad. Sci. USA 85, 4066–4070.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Dorn, A., Bernstein, H.G., Rinne, A., Hahn, H.J., and Ziegler, M. (1982). Insulin-like immunoreactivity in the human brain. Histochemistry 74, 293–300.

    Article  PubMed  CAS  Google Scholar 

  • Ernfors, P., Hallbook, F., Ebendal, T., Shooter, E.M., Radeke, M.J., Misko, T.P., and Persson, H. (1988). Developmental and regional expression of β-nerve growth factor receptor mRNA in the chick and rat. Neuron 1, 983–996.

    Article  PubMed  CAS  Google Scholar 

  • Esch, F., Baird, A., Ling, N., Ueno, N., Hill, F., Denoroy, L., Klepper, R., Gospodarowicz, D., Bohlen, P., and Guillemin, R. (1985). Primary structure of bovine pituitary basic fibroblast growth factor (FGF) and comparison with the amino-terminal sequence of bovine brain acidic FGF. Proc. Natl. Acad. Sci. USA 82, 6507–6511.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Gensburger, C., Labourdette, G., and Sensenbrenner, M. (1987). Brain basic fibroblast growth factor stimulates the proliferation of rat neuronal precursor cells in vitro. FEBS Lett. 217, 1–5.

    Article  PubMed  CAS  Google Scholar 

  • Gnahn, H., Hefti, F., Heumann, R., Schwab, M., and Thoenen, H. (1983). NGF-mediated increase of choline acetyltransferase (ChAT) in the neonatal forebrain: Evidence for a physiological role of NGF in the brain? Dev. Brain Res. 9, 45–52.

    Article  CAS  Google Scholar 

  • Hartikka, J., and Hefti, F. (1988a). Development of septal cholinergic neurons in culture: plating density and glial cells modulate effects of NGF on survival, fiber growth, and expression of transmitter-specific enzymes. J. Neurosci. 8, 2967–2985.

    PubMed  CAS  Google Scholar 

  • Hartikka, J., and Hefti, F. (1988b). Comparison of nerve growth factor’s effects on development of septum, striatum, and nucleus basalis cholinergic neurons in vitro. J. Neurosci. Res. 21, 352–364.

    Article  PubMed  CAS  Google Scholar 

  • Hatanaka, H., Tsukui, H., and Nihonmatsu, I. (1988). Developmental change in the nerve growth factor action from induction of choline acetyltransferase to promotion of cell survival in cultured basal forebrain cholinergic neurons from postnatal rats. Dev. Brain Res. 39, 88–95.

    Article  Google Scholar 

  • Hatten, M.E., Lynch, M., Rydel, R.E., Sanchez, J., Joseph-Silverstein, J., Moscatelli, D., Rifkin D. (1988). In vitro neurite extension by granule neurons is dependent upon astroglial-derived fibroblast growth factor. Dev. Biol. 125, 280–289.

    Article  PubMed  CAS  Google Scholar 

  • Hefti, F., Hartikka, J., Eckenstein, F., Gnahn, H., Heumann, R., and Schwab, M. (1985). Nerve growth factor (NGF) increases choline acetyltransferase but not survival or fiber outgrowth of cultured fetal septal cholinergic neurons. Neuroscience 14, 55–68.

    Article  PubMed  CAS  Google Scholar 

  • Hefti, F., Hartikka, J., and Knusel, B. (1989). Function of neurotrophic factors in the adult and aging brain and their possible use in the treatment of neurodegenerative diseases. Neurobiol. Aging, in press.

    Google Scholar 

  • Hill, J.M., Lesniak, M.A., Pert, C.B., and Roth, J. (1986). Autoradiographic localization of insulin receptors in rat brain: prominence in olfactory and limbic areas. Neuroscience 17, 1127–1138.

    Article  PubMed  CAS  Google Scholar 

  • Johnston, M.V., Rutkowski, J.L., Wainer, B.H., Long, J.B., and Mobley, W.C. (1987). NGF effects on developing forebrain cholinergic neurons are regionally specific. Neurochem. Res. 12, 985–994.

    Article  PubMed  CAS  Google Scholar 

  • Knusel, B., and Hefti, F. (1988). Nerve growth factor promotes development of rat forebrain but not pedunculopontine cholinergic neurons in vitro; lack of effect of ciliary neuronotrophic factor and retinoic acid. J. Neurosci. Res. 21, 365–375.

    Article  PubMed  CAS  Google Scholar 

  • Kyriakis, J.M., Hausman, R.E., and Peterson, S.W. (1987). Insulin stimulates choline acetyltransferase activity in cultured embryonic chicken retina neurons. Proc. Natl. Acad. Sci. USA 84, 7463–7467.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Large, T.H., Weskamp, G., Helder, J.C., Radeke, M.J., Misko, T.P., Shooter, E.M., and Reichardt, L.F. (1989). Structure and developmental expression of the nerve growth factor receptor in the chicken central nervous system. Neuron 2, 1123–1134.

    Article  PubMed  CAS  Google Scholar 

  • Manthorpe, M., Skaper, S.D., Williams, L.R., and Varon, S. (1986). Purification of adult rat sciatic nerve ciliary neuronotrophic factor. Brain Res. 367, 282–286.

    Article  PubMed  CAS  Google Scholar 

  • Martinez, H.J., Dreyfus, C.F., Jonakait, G.M., and Black, I.B. (1987). Nerve growth factor selectively increases cholinergic markers but not neuropeptides in rat basal forebrain in culture. Brain Res. 412, 295–301.

    Article  PubMed  CAS  Google Scholar 

  • Mobley, W.C, Rutkowski, J.L., Tennekoon, G.I., Gemski, J., Buchanan, K., and Johnston, M.V. (1986). Nerve Growth Factor increases choline acetyltransferase activity in developing basal forebrain neurons. Mol. Brain Res. 1, 53–62.

    Article  Google Scholar 

  • Monard, D. (1987) Role of protease inhibition in cellular migration and neuritic growth. Biochem. Pharmacol. 36, 1389–1392.

    Article  PubMed  CAS  Google Scholar 

  • Morrison, R.S., Keating, R.F., and Moskal, J.R. (1988). Basic fibroblast growth factor and epidermal growth factor exert differential trophic effects on CNS neurons. J. Neurosci. Res. 21, 71–79.

    Article  PubMed  CAS  Google Scholar 

  • Morrison, R.S. Kornblum, H.I., Leslie, F.M., and Bradshaw, R.A. (1987). Trophic stimulation of cultured neurons from neonatal rat brain by epidermal growth factor. Science 238, 72–75.

    Article  PubMed  CAS  Google Scholar 

  • Morrison, R.S., Sharma, A., DeVellis, J., and Bradshaw, R.A. (1986). Basic fibroblast growth factor supports the survival of cerebral cortical neurons in primary culture. Proc. Natl. Acad. Sci. USA 83, 7537–7541.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Otto, D., Frotscher, M., and Unsicker, K. (1989). Basic fibroblast growth factor and nerve growth factor administered in gel foam rescue medial septal neurons after fimbria fornix transection. J. Neurosci. Res. 22, 83–91.

    Article  PubMed  CAS  Google Scholar 

  • Puro, D.G., Agardh, E. (1984). Insulin-mediated regulation of neuronal maturation. Science 225, 1170–1172.

    Article  PubMed  CAS  Google Scholar 

  • Purves, D. (1986). The trophic theory of neural connections. Trends Neurosci. 9, 486–489.

    Article  Google Scholar 

  • Recio-Pinto, E., Rechter, M.M., and Ishii, D.N. (1986). Effects of insulin, insulin-like growth factor-II and nerve growth factor on neurite formation and survival in cultured sympathetic and sensory neurons. J. Neurosci. 6, 1211–1219.

    PubMed  CAS  Google Scholar 

  • Rotwein, P., Burgess, S.K., Milbrandt, J.D., and Krause, J.E. (1988). Differential expression of insulin-like growth factor genes in rat central nervous system. Proc. Natl. Acad. Sci. USA 85, 265–269.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Rydel, R.E., and Greene, L.A. (1987). Acidic and basic fibroblast growth factors promote stable neurite outgrowth and neuronal differentiation in cultures of PC12 cells. J. Neurosci. 7, 3639–3653.

    PubMed  CAS  Google Scholar 

  • Sara, V.R., Hall, K., von Holtz, H., Humber, R., Sjogren, B., and Wetterberg, L. (1982). Evidence for the presence of specific receptors for insulin-like growth factors 1 (IGF-1) and 2 (IGF-2) and insulin throughout the adult human brain. Neurosci. Lett. 34, 39–44.

    Article  PubMed  CAS  Google Scholar 

  • Schatteman, G.C., Gibbs, L., Lanahan, A.A., Claude, P., and Bothwell, M. (1988). Expression of NGF receptor in the developing and adult primate central nervous system. J. Neurosci. 8, 860–873.

    PubMed  CAS  Google Scholar 

  • Schubert, D., Ling, N., and Baird, A. (1987). Multiple influences of a heparin-binding growth factor on neuronal development. J. Cell Biol. 104, 635–643.

    Article  PubMed  CAS  Google Scholar 

  • Squire, L.R., and Davis, H.P. (1981). The pharmacology of memory: A neurobiological perspective. Annu. Rev. Pharmacol. Toxicol. 21, 323–356.

    Article  PubMed  CAS  Google Scholar 

  • Thoenen, H., and Edgar, D. (1985). Neurotrophic factors. Science 229, 238–242.

    Article  PubMed  CAS  Google Scholar 

  • Thoenen, H., Bandtlow, C., and Heumann, R. (1987). The physiological function of nerve growth factor in the central nervous system: comparison with the periphery. Rev. Physiol. Biochem. Pharmacol. 109, 145–178.

    PubMed  CAS  Google Scholar 

  • Togari, A., Dickens, G., Kuzuya, J., and Guroff, G. (1985). The effect of fibroblast growth factor on PC12 cells. J. Neurosci. 5, 307–316.

    PubMed  CAS  Google Scholar 

  • Unsicker, K., Reichert-Preibsch, H., Schmidt, R., Pettmann, B., Labourdette, G., and Sensenbrenner, M. (1987). Astroglial and fibroblast growth factors have neurotrophic functions for cultured peripheral and central nervous system neurons. Proc. Natl. Acad. Sci. USA 84, 5459–5463.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Varon, S., and Adler, R. (1980). Nerve growth factors and control of nerve growth. Curr. Top. Dev. Biol. 16, 207–252.

    Article  PubMed  CAS  Google Scholar 

  • Veomett, G., Kuszynski, C., Kazakoff, P., and Rizzino, A. (1989). Cell density regulates the number of cell surface receptors for fibroblast growth factor. Biochem. Biophys. Res. Comm. 159, 694–700.

    Article  PubMed  CAS  Google Scholar 

  • Walicke, P. Cowan, W.M., Ueno, N., Baird, A., and Guillemin, R. (1986). Fibroblast growth factor promotes survival of dissociated hippocampal neurons and enhances neurite extension. Proc. Natl. Acad. Sci. USA 83, 3012–3016.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Walicke, P.A., Feige, J.-J., and Baird, A. (1989). Characterization of the neuronal receptor for basic fibroblast growth factor and comparison to receptors in mesenchymal cells. J. Biol. Chem. 264, 4120–4126.

    PubMed  CAS  Google Scholar 

  • Walicke, P.A. (1988). Basic and acidic fibroblast growth factors have trophic effects on neurons from multiple CNS regions. J. Neurosci. 8, 2618–2627.

    PubMed  CAS  Google Scholar 

  • Walicke, P.A., and Baird, A. (1988). Neurotrophic effects of basic and acidic fibroblast growth factors are not mediated through glial cells. Dev. Brain Res. 40, 71–79.

    Article  CAS  Google Scholar 

  • Whittemore, S.R., and Seiger, A. (1987). The expression, localization and functional significance of beta-nerve growth factor in the central nervous system. Brain Res. Rev. 12, 439–464.

    Article  CAS  Google Scholar 

  • Woolf, N.J., and Butcher, L.L., (1986). Cholinergic systems in the rat brain: III. Projections from the pontomesencephalic tegmentum to the thalamus, tectum, basal ganglia, and basal forebrain. Brain Res. Bull. 16, 603–637.

    Article  PubMed  CAS  Google Scholar 

  • Yan, Q., and Johnson, E.M. (1988). An immunohistochemical study of the nerve growth factor receptor in developing rats. J. Neurosci. 8, 3481–3498.

    PubMed  CAS  Google Scholar 

Download references

Authors
  1. F. Hefti
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. B. Knusel
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. Department of Medical Cell Research, University of Lund, Sweden

    Anders Björklund

  2. Center for Research in Neuroscience, Montreal General Hospital, Canada

    Albert J. Aguayo

  3. Wenner-Gren Center Foundation, Stockholm, Sweden

    David Ottoson

Copyright information

© 1990 The contributors

About this chapter

Cite this chapter

Hefti, F., Knusel, B. (1990). Trophic Control of Central Cholinergic Neuron Development In Vitro. In: Björklund, A., Aguayo, A.J., Ottoson, D. (eds) Brain Repair. Wenner-Gren Center International Symposium Series. Palgrave, London. https://doi.org/10.1007/978-1-349-11358-3_2

Download citation

  • DOI: https://doi.org/10.1007/978-1-349-11358-3_2

  • Publisher Name: Palgrave, London

  • Print ISBN: 978-1-349-11360-6

  • Online ISBN: 978-1-349-11358-3

  • eBook Packages: EngineeringEngineering (R0)

Publish with us

Policies and ethics

Search

Navigation