Influence of Gangliosides and Nerve Growth Factor on the Plasticity of Forebrain Cholinergic Neurons

  • A. Claudio Cuello
  • D. Maysinger
  • L. Garofalo
  • P. Tagari
  • P. H. Stephens
  • E. Pioro
  • M. Piotte
Part of the Wenner-Gren Center International Symposium Series book series (WGS)

Abstract

Neurons from the medial septal nucleus and nucleus of the vertical limb of the diagonal band of Broca provide an important cholinergic input to the hippocampus (Lewis and Shute, 1967; Oderfeld-Nowak et al, 1974; Meibach and Siegel, 1977). The cortex receives a widespread distribution of cholinergic fibres, the majority of which seem to originate from the nucleus basalis magnocellularis (NBM) (Johnston et al, 1981; Fibiger, 1982; Cuello and Sofroniew, 1984). From immunohistochemical studies it would appear that a topographic representation exists for this projection (Mesulam et al, 1986; Ingham et al, 1985). These fibers represent approximately 70% of the total cholinergic component of the cortex (Lehman et al, 1982), the remainder deriving from local circuit neurons (Sofroniew et al, 1982; Johnston et al, 1981). This participation of forebrain cholinergic neurons has been emphasized in recent years since a decrease in choline acetyltransferase (ChAT) activity has been reported to occur in the cortex and in the NBM of patients with Alzheimer’s disease Bowen et al, 1983; Davies and Maloney, 1976; Perry et al, 1977; Rossor et al, 1982; Sims et al, 1983). Furthermore, a reduced number of cells in the latter area has been reported as a feature of Alzheimer’s disease (Whitehouse et al, 1982). On the basis of

Keywords

Tyrosine Dementia Shrinkage Choline Crest 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Beal, M.F., Benoit, R., Mazurek, M.F., Bird, E.D. and Martin, J.B. (1986). Somatostatin-281-12-like immunoreactivity is reduced in Alzheimer’s disease cerebral cortex. Brain Res., 368, 380–383.PubMedCrossRefGoogle Scholar
  2. Bitensky, M.W., Wheeler, M.A., Mehta, H. and Miki, N. (1975). Cholera toxin activation of adenylate cyclase in cancer cell membrane fragments. Proc. Natl. Acad. Sci. U.S.A., 72, 2572–2576.PubMedPubMedCentralCrossRefGoogle Scholar
  3. Bowen, D.M., Allen, S.J., Benton, J.S., Goodhart, M.J., Haan, E.A., Palmer, A.M., Sims, N.R., Smith, D.D.T., Spillane, J.A., Esiri, M.M., Neary, D., Snowdon, J.B., Wilcock, G.K. and Davison, A.N. (1983). Biochemical assessment of serotonergic and cholinergic dysfunction and cerebral atrophy in Alzheimer’s disease. J. Neurochem., 41, 266–272.PubMedCrossRefGoogle Scholar
  4. Casamenti, F., Bracco, L., Bartolin, L. and Faper, G. (1985). Effects of ganglioside treatment in rats with a lesion of the cholinergic forebrain nuclei. Brain Res., 338, 45–52.PubMedCrossRefGoogle Scholar
  5. Cuello, A.C., Sofroniew, M.V. (1984). The anatomy of the CNS cholinergic neurons. TINS, 7,74–78.Google Scholar
  6. Cuello, A.C., Milstein, D., Wright, B., Bramwell, B., Priestley, J.V. and Jarvis, J. (1984). Development and application of a monoclonal rat peroxidase anti-peroxidases (PAP) immunocytochemical reagent. Histochemistry, 30, 257–261.CrossRefGoogle Scholar
  7. Cuello, A.C., Stephens, P.H., Tagari, P.D., Sofroniew, M.V. and Pearson, R.C.A. (1986). Retrograde changes in the nucleus basalis of the rat, caused by cortical damage, are prevented by exogenous ganglioside GM1. Brain Res. 376, 373–377.PubMedCrossRefGoogle Scholar
  8. Davies, P. and Maloney, A.J.F. (1976). Selective loss of central cholinergic neurons in Alzheimer’s Disease. Lancet, II, 1403.Google Scholar
  9. Davies, P., Katzman, R. and Terry, R.D. (1980). Reduced somatostatin-like immunoreactivity in cerebral cortex of cases of Alzheimer disease and Alzheimer senile dementia. Nature, 288, 279–280.PubMedCrossRefGoogle Scholar
  10. Deelers, N., Chatelain, P., Poss, A. and Ruysschaert, J.M. (1979). Specific interaction between follitropin and GM1 ganglioside incorporated into lipid membranes. Biochem. Biophys. Res. Comm., 89, 1102–1106.CrossRefGoogle Scholar
  11. Eckenstein, F. and Thoenen, H. (1982). Production of specific antisera and monoclonal antibodies in choline acetyltransferase. Characterization and use for identification of cholinergic neurons. EMBO J. 1, 363–368.PubMedGoogle Scholar
  12. Fibiger, H.C. (1982). The orgnaization and some projections of cholinergic neurons of the mammalian forebrain. Brain Res. Rev., 4, 327–388.CrossRefGoogle Scholar
  13. Gill, D.M. and King, C.A. (1975). The mechanism of action of cholera toxin in pigeon erythrocyte lysates. J. Cell Biol., 250, 6424–6432.Google Scholar
  14. Hefti, F.A., Dravid, A. and Hartikka, J. (1984). Chronic intraventricular injections of nerve growth factor elevate hippocampal choline acetyltransferase activity in adult rats with partial septo-hippocampal lesions. Brain Res., 293, 305–309.PubMedCrossRefGoogle Scholar
  15. Heumann, R., Schwab, M.E., Merkl, R. and Thoenen, H. (1984). Nerve growth factor (NGF) mediated induction of choline acetyltransferase (ChAT) in PC12 cells: evaluation of the site of action of NGF and the involvement of lysosomal degradation products of NGF. J. Neurosci., 4, 3039–3050.PubMedGoogle Scholar
  16. Holmgren, J., Lonnroth, I., Mansson, J.E. and Svennerholm, L. (1975). Interaction of cholera toxin and membrane GM1 ganglioside of small intestine. Proc. Natl. Acad. Sci. U.S.A., 72, 2520–2524.Google Scholar
  17. Ingham, C.A., Bolam, J.P., Wainer, B.H. and Smith, A.D. (1985). A correlated light and electron microscopic study of identified cholinergic basal forebrain neurons that project to the cortex in the rat. J. Comp. Neurol., 239, 176–192.PubMedCrossRefGoogle Scholar
  18. Johnston, M.V., McKinney, M. and Coyle, J.T. (1981). Neocortical cholinergic innervation: A description of extrinsic and intrinsic components in the rat. Brain Res., 43, 159–172.Google Scholar
  19. Korshing, S. and Thoenen, H. (1983). Quantitative demonstartion of the retrograde axonal transport of endogenous nerve growth factor. Neurosci. Lett., 39, 1–4.CrossRefGoogle Scholar
  20. Kurosky, A., Markel, D.E., Peterson, J.W. and Fitch, W.M. (1977). Primary structure of cholera toxin β-chain: A glycoprotein hormone analog? Science, 195, 299–301.PubMedCrossRefGoogle Scholar
  21. Lehman, J., Nagy, J.I., Almadja, S. and Fibiger, H.C. (1982). The nucleus basalis magnocellularis; the origin of a cholinergic projection to the neocortex in the rat. Neuroscience, 5, 1161– 1174.Google Scholar
  22. Lewis, P.R. and Shute, C.C.D. (1967). The cholinergic limbic system: Projections to hippocampal formation, medial cortex, nuclei of the ascending cholinergic reticular system and the subfornical organ and supra-optic crest. Brain, 90, 521–540.PubMedCrossRefGoogle Scholar
  23. Meibach, R.C. and Siegel, A. (1977) Efferent connections of the hippocampal formation in the rat. Brain Res., 124, 197–224.PubMedCrossRefGoogle Scholar
  24. Mesulam, M., Mufson, E.J. and Wainer, B.H. (1986). Three-dimensional representation and cortical projection topography of the nucleus basalis (Ch4) in the macaque: concurrent demonstration of choline acetyltransferase and retrograde transport with a stabilised tetramethylbenzidine method for horseradish peroxidase. Brain Res., 367, 301–308.PubMedCrossRefGoogle Scholar
  25. 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.CrossRefGoogle Scholar
  26. Morrison, J.H., Rogers, J., Scherr, S., Benoit, R. and Bloom, F.E. (1985). Somatostatin immunoreactivity in neuritic plaques of Alzheimer’s patients. Nature, 314, 90–92PubMedCrossRefGoogle Scholar
  27. Mullin, B.R., Fishman, P.H., Lee, G., Aloj, S.M., Ledley, F.D., Winand, R.J., Kohn, L.D. and Brady, R.O. (1976). Thyrotropin-ganglioside interactions and their relationship to the structure and function of thyrotripin receptor. Proc. Natl. Acad. Sci. U.S.A., 73, 842–846.PubMedPubMedCentralCrossRefGoogle Scholar
  28. Nieto-Sampedro, M., Lewis, E.R., Cotman, C.W., Manthorpe, E.M., Skaper, S.D., Barbin, G., Longo, F.M. and Waron, S. (1982). Brain injury causes a time dependent increase in neuron trophic activity at the lesion site. Science 217,860–861.Google Scholar
  29. Oderfeld-Nowak, B., Narkiewicz, O., Bialowas, J., Wieraszko, A. and Gradkowska, M. (1974). The influence of septal nuclei lesions on activity of acetylcholinesterase and choline acetyltransferase in the hippocampus of the rat. Acta Neurobiol. Exp. 34, 583–601.Google Scholar
  30. Oderfeld-Nowak, B., Skup, M., Ulas, J., Jezierska, M., Gradkowska, R. and Zaremba, M. (1984). Effect of GM1 ganglioside treatment on post lesion responses of cholinergic neurons in rat hippocampus after various partial deafferentations. J. Neurosci. Res., 12, 409–420.PubMedCrossRefGoogle Scholar
  31. Perry, E.R., Perry, R.H., Blessed, G. and Roth, M. (1977). Necropsy evidence of central cholinergic deficits in senile dementia. Lancet, I,189.Google Scholar
  32. Richardson, P.M., Verge-Issa, V.M.K. and Riopelle, R.J. (1986). Distribution of neuronal receptors for nerve growth factor in the rat. J. Neurosci., 6, 2312–2321.PubMedGoogle Scholar
  33. Roberts, G.W., Crow, T.J. and Polak, J.M. (1985). Location of neuronal tangles in somatostatin neurons in Alzheimer’s disease. Nature, 314, 92–94.PubMedCrossRefGoogle Scholar
  34. Rossor, M.N., Garret, N.J., Johnson, A.L., Mountjoy, D.Q., Roth, M. and Iversen, L.L. (1982b). A post-mortem study of the cholinergic and GABA systems in senile dementia. Brain, 185, 313–330.CrossRefGoogle Scholar
  35. Schwab, M.E., Otten, U., Agid, Y. and Thoenen, H. (1979). Nerve growth factor (NGF) in the rat CNS: absence of specific retrograde axonal transport and tyrosine hydroxylase induction in locus coeruleus and substantia nigra. Brain Res., 168, 473–483.PubMedCrossRefGoogle Scholar
  36. Sims, N.R., Bowen, D.M., Allan, S.J., Smith, C.C.T., Neary, D., Thomay, D.J. and Davison, A.N. (1983). Presynaptic cholinergic dysfunction in patients with dementia. J. Neurochem., 401 503– 509.Google Scholar
  37. Smith, R.G. and Appel, S.H. (1983). Extracts of skeletal muscle increase neurite outgrowth and cholinergic activity of fetal rat spinal motor neurons. Science, 219, 1079–1081.PubMedCrossRefGoogle Scholar
  38. Smith, R.G., McManaman, J. and Appel, S.H. (1986). Trophic effects of skeletal muscle extracts on ventral spinal cord neurons in vitro separation of a protein with morphologic activity from proteins with cholinergic activity. J. Cell Biol., 101, 1608–1621.CrossRefGoogle Scholar
  39. Smith, R.G., Vaca, K., McManaman, J. and Appel, S.H. (1985). Selective effects of skeletal muscle extract fractions on motoneuron development in vitro. J. Neurosci., 6, 439–447.Google Scholar
  40. Sofroniew, M.V., Eckenstein, F., Thoenen, H. and Cuello, A.C. (1982). Topography of choline acetyltransferase-containing neurons in the forebrain of the rat. Neurosci. Lett., 33, 7–12.PubMedCrossRefGoogle Scholar
  41. Sofroniew, M.V., Pearson, R.C.A., Cuello, A.C., Stevens, P.H. and Tagari P. (1986). The effect of parenterally administered GM1 ganglioside on retrograde degeneration of cholinergic cells of the basal forebrain of the rat. Brain Res., 398, 393–396.PubMedCrossRefGoogle Scholar
  42. Sofroniew, M.V., Pearson, R.C.A., Eckenstein, F., Cuello, A.C. and Powell, T.P.S. (1983). Retrograde changes in cholinergic neurons in the basal forebrain of the rat following cortical damage. Brain Res., 289, 370–374.PubMedCrossRefGoogle Scholar
  43. Stephens, P.H., Cuello, A.C., Sofroniew, M.V., Pearson, R.D.A. and Tagari, P. (1985). The effect of unilateral decortication upon choline acetyltransferase and glutamate decarboxylase activities in the nucleus basalis and other areas of the rat brain. J. Neurochem., 45, 1021–1026.PubMedCrossRefGoogle Scholar
  44. Stephens, P.H., Tagari, P.C. and Cuello, A.C. (1987). Cholinergic neurons in aged rats: changes after cortical lesions. Neurobiol. Aging (submitted).Google Scholar
  45. Tanuichi, M., Schweitzer, J.B. and Johnson, E.M. (1986). Nerve growth factor receptor molecules in rat brain. Proc. Natl. Acad. Sci., 83, 1950–1954.CrossRefGoogle Scholar
  46. Toffano, G., Benvegnu, D., Bonetti, A.C., Facci, L., Leon, A., Orlando, P., Ghidoni, R. and Tettamanti, G. (1980). Interactions of GM1 ganglioside with crude rat brain neuronal membranes. J. Neurochem., 35, 861–866.PubMedCrossRefGoogle Scholar
  47. Van Heyningen, S. (1974). Cholera toxin: Interaction of subunits with ganglioside GM1. Science, 183, 656–666.CrossRefGoogle Scholar
  48. Wenk, G.L. and Olton, D.S. (1984). Recovery of neocortical ChAT activity following ibotenic acid injection into the nucleus basalis of Meynert in rats. Brain Res., 293, 184–186.PubMedCrossRefGoogle Scholar
  49. Whitehouse, P.J., Price, D.L., Strubie, R.G., Clark, A.W., Coyle, J.T. and DeLong, M.R. (1982). Alzheimer’s disease and senile dementia loss of neurons in the basal forebrain. Science, 215, 1237–1239.PubMedCrossRefGoogle Scholar
  50. Williams, L.R., Peterson, G.M., Varon, S. and Gage, F.H. (1986). Continuous infusion of NGF prevents non-cholinergic as well as cholinergic neuronal death in the medial septum after fimbria formix transection. Society for Neuroscience 16th Annual Meeting, Washington, November 9–14, 1986, Abstr. 219.3, page 787.Google Scholar
  51. Wojcik, M., Ules, J. and Oderfeld-Nowak, B. (1982). The stimulating effect of ganglioside injections on the recovery of choline acetyltransferase and acetylcholinesterase activities in the hippocampus of the rat after septal lesions. Neuroscience, 7,495–499.Google Scholar

Copyright information

© The Wenner-Gren Center 1987

Authors and Affiliations

  • A. Claudio Cuello
  • D. Maysinger
  • L. Garofalo
  • P. Tagari
  • P. H. Stephens
  • E. Pioro
  • M. Piotte

There are no affiliations available

Personalised recommendations