Neurotrophic Factors Produced by Astrocytes involved in the Regulation of Cholinergic Neurons in the Central Nervous System

  • Ambrish J. Patel
  • Carol W. Gray
Part of the Altschul Symposia Series book series (ALSS, volume 2)

Abstract

The importance of the interaction between astrocytes and neurons, mediated by functionally active cellular constituents, is well documented for the normal development of the brain (Sensenbrenner and Mandel, 1974; Varon and Somjen, 1979; Banker, 1980; Silver and Ogawa, 1983; Denis-Donini et al., 1984; Rakic, 1985; Rudge et al., 1985; Hatten et al., 1988; Hayashi et al., 1988; Patel and Hunt, 1989). These earlier studies have shown that diffusible and/or membrane bound factors produced by astrocytes affect the survival, migration, axonal growth and specific morphological patterns of neurons. However, in the majority of these studies, the trophic effect of astrocytes has been examined on uncharacterized neurons, rather than on a defined population of nerve cells. Since our initial observations showing the production by astrocytes of a trophic factor important in the maintenance of metabolic status and physiological functions of cholinergic neurons (Patel et al., 1988b; Patel and Hunt, 1989), several astrocytic trophic molecules have been characterized as influencing various neuronal populations.

Keywords

Nerve Growth Factor Neurotrophic Factor Basic Fibroblast Growth Factor Cholinergic Neuron Basal Forebrain 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 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.PubMedCrossRefGoogle Scholar
  2. Araujo, D.M., and Cotman, C.W., 1992, ß-amyloid stimulates glial cells in vitro to produce growth factors that accumulate in senile plaques in Alzheimer’s disease, Brain Res. 569: 141.PubMedCrossRefGoogle Scholar
  3. Arendt, T., Allen, Y., Marchbanks, R.M., Schugens, M.M., Lantos, P.L., and Gray, J.A., 1989, Cholinergic system and memory in the rat: effects of chronic ethanol, embryonic basal forebrain transplants and excitotoxic lesions of cholinergic basal forebrain projection systems, Neuroscience 33: 435.PubMedCrossRefGoogle Scholar
  4. Azmitia, E.C., Dolan, K., and Whitaker-Azmitia, P.M., 1990, S-100p but not NGF, EGF, insulin or calmodulin is a CNS serotonergic growth factor, Brain Res. 516: 354.PubMedCrossRefGoogle Scholar
  5. Baird, A., and Bohlen, P., 1990, Fibroblast growth factors, Handb. Expl.Pharmacol. 95 /1: 369.CrossRefGoogle Scholar
  6. Bakhit, C., Armanini, M., Bennett, G.L., Wong, W.L.T., Hansen, S.E., and Taylor, R., 1991, Increase in glia-derived nerve growth factor following destruction of hippocampal neurons, Brain Res. 560: 76.PubMedCrossRefGoogle Scholar
  7. Banker, G.A., 1980, Trophic interactions between astroglial cells and hippocampal neurons in culture, Science 209: 809.PubMedCrossRefGoogle Scholar
  8. Barde, Y-A., 1989, Trophic factors and neuronal survival, Neuron 2: 1525.Google Scholar
  9. Barres, B.A., Chun, L.L.Y., and Corey, D.P., 1990, Ion channels in vertebrate glia, Ann. Rev. Neurosci. 13: 441.PubMedCrossRefGoogle Scholar
  10. Belin, D., Wohlwend, A., Schleuning, W-D., Kruithof, E.K.O., and Vassalli, J-D., 1989, Facultative polypeptide translocation allows a single mRNA to encode the secreted and cytosolic forms of plasminogen activators inhibitor 2, EMBO J. 8: 3287.PubMedGoogle Scholar
  11. Berkemeier, L.R., Winslow, J.W., Kaplan, D.R., Nikolics, K., Goeddel, D.V., and Rosenthal, A., 1991, Neurotrophin-5: a novel neurotrophic factor that activates trk and trkB, Neuron 7: 857.PubMedCrossRefGoogle Scholar
  12. Caday, C.G., Klagsbrun, M., Fanning, P.J., Mirzabegian, A., and Finklestein, S.P., 1990, Fibroblast growth factor (FGF) levels in the developing rat brain, Dev. Brain Res. 52: 241.CrossRefGoogle Scholar
  13. Cras, P., Kawai, M., Siedlak, S., and Perry, G., 1991, Microglia are associated with extracellular neurofibrillary tangles of Alzheimer disease, Brain Res. 558: 312.PubMedCrossRefGoogle Scholar
  14. Decker, M.W., 1987, The effects of aging on hippocampal and cortical projections of the forebrain cholinergic systems, Brain Res. Rev. 12: 423.CrossRefGoogle Scholar
  15. Denis-Donini, S., Glowinski, J., and Prochiantz, A., 1984, Glial heterogeneity may define the threedimensional shape of mouse mesencephalic dopaminergic neurons, Nature 307: 641.PubMedCrossRefGoogle Scholar
  16. Dunnett, S.B., Low, W.C., Iversen, D., Stenevi, U., and Bjorklund, A., 1982, Septal transplants restore maze learning in rats with fimbria-fomix lesions, Brain Res. 251: 335.PubMedCrossRefGoogle Scholar
  17. Ferguson, I.A., Schweitzer, J.B., and Johnson, E.M., Jr., 1990, Basic fibroblast growth factor: receptor-mediated internalization, metabolism, and anterograde axonal transport in retinal ganglion cells, J. Neurosci. 10: 2176.PubMedGoogle Scholar
  18. Fischer, W., Wictorin, K., Bjorklund, A., Williams, L.R., Varon, S., and Gage, F.H., 1987, Amelioration of cholinergic neuron atrophy and spatial memory impairment in aged rats by nerve growth factor, Nature 329: 65.PubMedCrossRefGoogle Scholar
  19. Frautschy, S.A., Walicke, P.A., and Baird, A., 1991, Localization of basic fibroblast factor and its mRNA after CNS injury, Brain Res. 553: 291.PubMedCrossRefGoogle Scholar
  20. Fukumoto, H., Kakihana, M., and Suno, M., 1991, Recombinant human basic fibroblast growth factor (thbFGF) induces secretion of nerve growth factor (NGF) in cultured rat astroglial cells, Neurosci. Lett. 122: 221.PubMedCrossRefGoogle Scholar
  21. Furukawa, S., Furukawa, Y., Satoyoshi, E., and Hayashi, K., 1987, Regulation of nerve growth factor synthesis/secretion by catecholamine in cultured mouse astroglial cells, Biochem. Biophys. Res. Commun. 147: 1048.PubMedCrossRefGoogle Scholar
  22. Furukawa, Y., Tomioka, N., Sato, W., Satoyoshi, E., Hayashi, K., and Furukawa, S., 1989, Catecholamines increase nerve growth factor mRNA content in both mouse astroglial cells and fibroblast cells, FEBS Lett. 247: 463.PubMedCrossRefGoogle Scholar
  23. Gage, F.H., Bjorklund, A., Stenevi, U., Dunnett, S.B., and Kelly, P.A.,1984, Intrahippocampal septal grafts ameliorate learning impairments in aged rats, Science 225: 533.Google Scholar
  24. Gnahn, H., Hefti, F., Heumann, R., Schwab, M.E., and Thoenen, H., 1983, NGF-mediated increase of choline acetyltransferase (ChAT) in the neonatal rat forebrain; evidence for a physiological role of NGF in the brain? Dev. Brain Res. 9: 45.CrossRefGoogle Scholar
  25. Gospodarowicz, D., Ferrara, N., Schweigerer, L., and Neufeld, G., 1987, Structural characterization and biological functions of fibroblast growth factor, Endocrinol. Rev. 8: 95.CrossRefGoogle Scholar
  26. Gray, C., and Patel, A.J., 1991, Further characterization of cholinergic factor produced by primary cultures of astrocytes, Eur. J. Neurosci. Suppl. 4: 286.Google Scholar
  27. Gray, C., and Patel, A.J., 1992, Characterization of a neurotrophic factor produced by cultured astrocytes involved in the regulation of subcortical cholinergic neurons, Brain Res. 574: 257.PubMedCrossRefGoogle Scholar
  28. Griffin, W.S.T., Stanley, L.C., Ling, C., White, L., MacLeod, V., Perrot, L.J., White, C.L., and Araoz, C., 1989, Brain interleukin-1 and S-100 immunoreactivity are elevated in Down syndrome and Alzheimer’s disease, Proc. Natl. Acad. Sci. U.SA. 86: 7611.CrossRefGoogle Scholar
  29. Grothe, C., Otto, D., and Unsicker, K., 1989, Basic fibroblast growth factor promotes in vitro survival and cholinergic development of rat septal neurons: comparison with the effect of nerve growth factor, Neuroscience 31: 649.PubMedCrossRefGoogle Scholar
  30. Hatten, M.E., Lynch, M., Rydel, R.E., Sanchez, J., Silverstein, J., Moscatelli, D., and Rifkin, D.B., 1988, In vivo neurite extension by granule neurons is dependent upon astroglial-derived fibroblast growth factor, Dev. Biol. 125: 280.Google Scholar
  31. Hayashi, M., and Patel, A.J., 1987, An interaction between thyroid hormone and nerve growth factor in the regulation of choline acetyltransferase activity in neuronal cultures, derived from the septal-diagonal band region of the embryonic rat brain, Dev. Brain Res. 36: 109.CrossRefGoogle Scholar
  32. Hayashi, M., Hayashi, R., Tanii, H., Hashimoto, K., and Patel, A.J., 1988, The influence of neuronal cells on the development of glutamine synthetase in astrocytes in vitro, Dev. Brain Res. 41: 37.CrossRefGoogle Scholar
  33. Hefti, F., Hartikka, J., Eckenstein, F., Gnahn, H., Heumann, R., and Schwab, M., 1985, Nerve growth factor increases choline acetyltransferase but not survival or fiber outgrowth of cultured fetal septal cholinergic neurons, Neuroscience 14: 55.PubMedCrossRefGoogle Scholar
  34. 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 10: 515.PubMedCrossRefGoogle Scholar
  35. Hofmann, H.D., 1988, Ciliary neuronotrophic factor stimulates choline acetyltransferase activity in cultured chicken retina neurons, J. Neurochem. 51:109.Google Scholar
  36. Houlgatte, R., Mallat, M., Brachet, P., and Prochiantz, A., 1989, Secretion of nerve growth factor in culture of glial cells and neurons derived from different regions of the mouse brain, J. Neurosci. Res. 24: 143.PubMedCrossRefGoogle Scholar
  37. Hyman, C., Hofer, M., Barde, Y-A., Juhasz, M., Yancopoulos, G.D., Squinto, S.P., and Lindsay, R.M., 1991, BDNF is a neurotrophic factor for dopaminergic neurons of the substantia nigra, Nature 350: 230.PubMedCrossRefGoogle Scholar
  38. Itagaki, S., McGeer, P.L., Akiyama, H., Zhu, S., and Selkoe, D., 1989, Relationship of microglia and astrocytes to amyloid deposits in Alzheimer’s disease, J. Neuroimmunol. 24: 173.PubMedCrossRefGoogle Scholar
  39. Kamegai, M., Niijima, K., Kunishita, T., Nishizawa, M., Ogawa, M., Araki, M., Ueki, A., Konishi, Y., and Tabira, T., 1990, Interleukin 3 as a trophic factor for central cholinergic neurons in vitro and in vivo, Neuron 4: 429.PubMedCrossRefGoogle Scholar
  40. Kimelberg, H.K., 1988, “Glial Cell Receptors,” Raven Press, New York.Google Scholar
  41. Kiss, J., McGovern, J., and Patel, A.J., 1988, Immunohistochemical localization of cells containing nerve growth factor receptors in the different regions of the adult rat forebrain, Neuroscience 27: 731.PubMedCrossRefGoogle Scholar
  42. Kiyota, Y., Takami, K., Iwane, M., Shino, A., Miyamoto, M., Tsukuda, R.,and Nagaoka, A., 1991, Increase in basic fibroblast growth factor-like immunoreactivity in rat brain after forebrain ischemia, Brain Res. 545: 322.Google Scholar
  43. Kostura, M.J., Tocci, M.J., Limjuco, G., Chin, J., Cameron, P., Hillman,A.G., Chartrain, N.A., and Schmidt, J.A., 1989, Identification of a monocyte specific pre-interleukin 1(i convertase activity, Proc. Natl. Acad. Sci. U.S.A. 86: 5227.CrossRefGoogle Scholar
  44. Large, T.H., Bodary, S.C., Clegg, D.O., Weskamp, G., Otten, U., and Reichardt, L.F., 1986, Nerve growth factor gene expression in the developing rat brain, Science 234: 352.PubMedCrossRefGoogle Scholar
  45. Levi, G., 1990, “Differentiation and Functions of Glial Cells,” Wiley-Liss, New York.Google Scholar
  46. Lindholm, D., Hengerer, B., Zafra, F., and Thoenen, H., 1990, Transforming growth factor-β1 stimulates expression of nerve growth factor in the rat CNS, NeuroReport 1:9. Logan, A., 1990, CNS growth factors, Br. J. Hosp. Med. 43: 428.Google Scholar
  47. Lyons, M.K., Anderson, R.E., and Meyer, F.B., 1991, Basic fibroblast growth factor promotes in vivo cerebral angiogenesis in chronic forebrain ischemia, Brain Res. 558: 315.PubMedCrossRefGoogle Scholar
  48. McManaman, J., Crawford, F., Clark, R., Richker, J., and Fuller, F., 1989, Multiple neurotrophic factors from skeletal muscle: demonstration of effects of basic fibroblast growth factor and comparisons with the 22KD choline acetyltransferase development factor, J. Neurochem. 53: 1763.PubMedCrossRefGoogle Scholar
  49. Mocchetti, L., De Bernardi, M.A., Szekely, A.M., Alho, H., Brooker, G., and Costa, E, 1989, Regulation of nerve growth factor biosynthesis by (i-adrenergic receptor activation in astrocytoma cells: a potential role of c-fos protein, Proc. Natl. Acad. Sci. U.SA. 86: 3891.CrossRefGoogle Scholar
  50. Neveu, I, Jehan, F., Houlgatte, R., Wion, D., and Brachet, P., 1992, Activation of nerve growth factor synthesis in primary glial cells by phorbol 12-myristate 13-acetate: role of protein kinase C, Brain Res. 570: 316.PubMedCrossRefGoogle Scholar
  51. Otto, D., and Unsicker, K., 1990, Basic FGF reverses chemical and morphological deficits in the nigrostriatal system of MPTP treated mice, J. Neurosci. 10: 1912.PubMedGoogle Scholar
  52. Otto, D., Frotscher, M., and Unsicker, K., 1989, Basic fibroblast growth factor and nerve growth factor administration in gel foam rescue medial septal neurons after fimbria fornix transection, J. Neurosci. Res. 22: 83.PubMedCrossRefGoogle Scholar
  53. Patel, A.J., 1986, Development of astrocytes: in vivo and in vitro studies, Adv. Biosci. 61: 87.Google Scholar
  54. Patel, A.J., and Hunt, A., 1989, Regulation of production by primary cultures of rat forebrain astrocytes of a trophic factor important for the development of cholinergic neurons, Neurosci. Lett. 99: 223.PubMedCrossRefGoogle Scholar
  55. Patel, A.J., Hayashi, M., and Hunt, A., 1988a, Role of thyroid hormone and nerve growth factor in the development of choline acetyltransferase and other cell-specific marker enzymes in the basal forebrain of the rat, J. Neurochem. 50: 803.PubMedCrossRefGoogle Scholar
  56. Patel, A.J., Hunt, A., and Seaton, P., 1988b, The mechanism of cytosine arabinoside toxicity on quiescent astrocytes in vitro appears to be analogous to in vivo brain injury, Brain Res. 450: 378.PubMedCrossRefGoogle Scholar
  57. Patel, A.J., Hunt, A., Gray, C.W., Kiss, J., and Sanfeliu, C., 1990, Neurotrophic factors produced by astrocytes influencing the development and normal functioning of cholinergic neurons, in: “Differentiation and Functions of Glial Cells,” G. Levi, ed., p. 123, Wiley-Liss, New York.Google Scholar
  58. Patel, A.J., Kiss, J., and Gray, C.W., 1992, Organisation of septo-hippocampal neurons and their regulation by trophic factors produced by astrocytes, in: “Neurodegeneration,” A.J. Hunter and M. Clark, eds., p. 59, Academic Press, London.Google Scholar
  59. Pettmann, B., Labourdette, G., Weibel, M., and Sensenbrenner, M., 1986, The brain fibroblast growth factor (FGF) is localized in neurons, Neurosci. Lett. 68: 175.PubMedCrossRefGoogle Scholar
  60. Quon, D., Catalano, R., and Cordell, B., 1990, Fibroblast growth factor induces ß-amyloid precursor mRNA in glial but not neuronal cultured cells, Biochem. Biophys. Res. Commun. 167: 96.PubMedCrossRefGoogle Scholar
  61. Rakic, P., 1985, Contact regulation of neuronal migration, in: “The Cell in Contact: Adhesions and Junctions as Morphogenetic Determinants,” G.M. Edleman and J.P. Thiery, eds., p. 67, Wiley, New York.Google Scholar
  62. Riva, M.A., and Mocchetti, I, 1991, Developmental expression of the basic fibroblast growth factor gene in rat brain, Dev. Brain Res. 62: 45.CrossRefGoogle Scholar
  63. Rosenberg, M.B., Friedmann, T., Robertson, R.C., Tuszynski, M., Wolff, J.A., Breakefield, X.O., and Gage, F.H., 1988, Grafting genetically modified cells to the damaged brain: restorative effects of NGF expression, Science 242: 1575.PubMedCrossRefGoogle Scholar
  64. Roth, M., and Iversen, L.L., eds., 1986, Alzheimer’s disease and related disorders, Br. Med. Bull. 42:1.Google Scholar
  65. Rudge, J.S., Manthorpe, M., and Varon, S., 1985, The output of neurotrophic and neurite promoting agents from rat brain astroglial cells: a microculture method of screening potential regulatory molecules, Dev. Brain Res. 19: 161.CrossRefGoogle Scholar
  66. Schwartz, J.P., and Mishler, K., 1990, Beta-adrenergic receptor regulation, through cyclic AMP, of nerve growth factor expression in rat cortical and cerebellar astrocytes, Cell Mol. Neurobiol. 18: 447.CrossRefGoogle Scholar
  67. Sendtner, M., Kreutzberg, G.W., and Thoenen, H., 1990, Ciliary neurotrophic factor prevents the degradation of motor neurons after axotomy, Nature 345: 440.PubMedCrossRefGoogle Scholar
  68. Sensenbrenner, M., and Mandel, P., 1974, Behaviour of neuroblasts in the presence of glial cells, fibroblasts and meningeal cells in culture, Exp. Cell Res. 87: 159.PubMedCrossRefGoogle Scholar
  69. Silver, J., and Ogawa, M.Y., 1983, Postnatally induced formation of the corpus callosum in acallosal mice on glia-coated cellulose bridge, Science 220: 1067.PubMedCrossRefGoogle Scholar
  70. Spranger, M., Lindholm, D., Bandtlow, C., Heumann, R., Gnahn, H., Naher-Noe, M., and Thoenen, H., 1990, Regulation of nerve growth factor (NGF) synthesis in the rat central nervous system: comparison between the effects of interleukin-1 and various growth factors in astrocyte cultures and in vivo, Eur. J. Neurosci. 2: 69.PubMedCrossRefGoogle Scholar
  71. Stockai, K.A., Lottspeich, F., Sendtner, M., Masiakowski, P., Carroll, P., Gotz, R., Lindholm, D., and Thoenen, H., 1989, Molecular cloning, expression and regional distribution of rat ciliary neurotrophic factor, Nature 342: 920.CrossRefGoogle Scholar
  72. Stopa, E.G., Gonzalez, A.M., Chorsky, R., Corona, R.J., Alvarez, J., Bird, E.D., and Baird, A., 1990, Basic fibroblast growth factor in Alzheimer’s disease, Biochem. Biophys. Res. Commun. 171: 690.Google Scholar
  73. Sweetnam, P.M., Sanon, H.R., White, L.A., Brass, B.J., Jaye, M., and Whittemore, S.R., 1991, Differential effects of acidic and basic fibroblast growth factors on spinal cord cholinergic, GABAergic, and glutamatergic neurons, J. Neurochem. 57: 237.PubMedCrossRefGoogle Scholar
  74. Thoenen, H., 1991, The changing scene of neurotrophic factors, Trends Neurosci. 14: 165.PubMedCrossRefGoogle Scholar
  75. Thomas, D., Groux-Muscatelli, B., Raes, M-B., Caruelle, J-P., Stehelin,D., Barritault, D., and Boilly, B., 1991, Developmental changes of acidic fibroblast growth factor (aFGF) transcription and expression in mouse brain, Des,. Brain Res. 59: 117.CrossRefGoogle Scholar
  76. Varon, S., and Somjen, G., 1979, Neuron glial interactions, Neurosci. Res. Progr. Bull. 17:1. Walicke, P.A., 1989, Novel neurotrophic factors, receptors, and oncogenes, Annu. Rev. Neurosci. 12: 103.Google Scholar
  77. Westermann, R., Grothe, C., and Unsicker, K., 1990, Basic fibroblast growth factor (bFGF), a multifunctional growth factor for neuroectodermal cells, J. Cell Sci. Suppl. 13: 97.PubMedGoogle Scholar
  78. Yayon, A., Klagsbrun, M., Esko, J.D., Leder, P., and Ornitz, D.M., 1991, Cell surface, heparin-like molecules are required for binding of basic fibroblast growth factor to its high affinity receptor, Cell 64: 841.PubMedCrossRefGoogle Scholar
  79. Yoshida, K., and Gage, F.H., 1991, Fibroblast growth factors stimulate nerve growth factor synthesis and secretion by astrocytes, Brain Res. 538: 118.PubMedCrossRefGoogle Scholar
  80. Yoshida, K., and Gage, F.H., 1992, Cooperative regulation of nerve growth factor synthesis and secretion in fibroblasts and astrocytes by fibroblast growth factor and other cytokines, Brain Res. 569: 14.PubMedCrossRefGoogle Scholar
  81. Zafra, F., Hengerer, B., Leibrock, J., Thoenen, H., and Lindholm, D., 1990, Activity dependent regulation of BDNF and NGF mRNAs in the rat hippocampus is mediated by non-NMDA glutamate receptors, EMBO J. 9: 3545.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1993

Authors and Affiliations

  • Ambrish J. Patel
    • 1
  • Carol W. Gray
    • 1
  1. 1.MRC Collaborative Centre and Division of Neurophysiology and NeuropharmacologyNational Institute for Medical ResearchLondonUK

Personalised recommendations