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Structure and Expression of ß-Nerve Growth Factor in the Rat Central Nervous System

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Neural Development and Regeneration

Part of the book series: NATO ASI Series ((ASIH,volume 22))

Abstract

Target-derived neuronal trophic factors have been implicated in the maturation and maintainance of both the central (CNS) and peripheral (PNS) nervous systems1-3 The most well characterized of these is β–nerve growth factor (NGF). The effects of NGF on PNS sensory and sympathetic neurons are well documented4,5 Present evidence suggests a physiological role for NGF also in the CNS. These data include the detection of molecules in the CNS with “NGF-like” physiological activity6-10 or immunological cross-reactivity9,11-15, as well as measurements of altered biological responses subsequent to injection of NGF or anti-NGF antibodies into the CNS16-25 Recent advances in recombinant DNA technology have allowed determination of NGF mRNA levels in the brain9,11,12,15,26-28. Finally, both the detection of specific NGF receptors in the CNS29-33 and the observed effects of NGF on cultured CNS neurons34-40 have supported a possible role of NGF in the CNS.

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References

  1. Cowan WM, Fawcett JW, O’Leary DDM Stanfield B. (1984) Regressive events in neurogenesis. Science 227:1258–1265

    Article  Google Scholar 

  2. Nieto-Sampedro M, Cotman CW (1985) Growth factor induction and temporal order in central nervous system repair. In: Cotman CW (ed) Synaptic Plasticity. Guilford, New York, p 407

    Google Scholar 

  3. Easter SS, Purves D, Rakic P, Spitzer NC (1985) The changing view of neural specificity. Science 230:507–511

    Article  PubMed  Google Scholar 

  4. Levi-Montalcini R, Angeletti PU (1968) Nerve qrcwth factor. Physiol Rev 48:534–569

    PubMed  CAS  Google Scholar 

  5. Thoenen H, Barde Y-A (1980) Physiology of nerve growth factor. Physiol Rev 60:1285–1335

    Google Scholar 

  6. Crutcher KA, Brothers L, Davis JN (1979) Sprouting of sympathetic nerves in the absence of afferent input. Exp Neurol 66:778–783

    Article  PubMed  CAS  Google Scholar 

  7. Crutcher KA, Collins F (1982) In vitro evidence for tvro distinct hippocampal growth factors: basis of neuronal plasticity? Science 217: 67–68

    Article  PubMed  CAS  Google Scholar 

  8. Collins F, Crutcher KA (1985) Neurotrophic activity in the adult rat hippocampal formation: rational distribution and increase after septal lesion. J Neurosci 5:2809–2814

    PubMed  CAS  Google Scholar 

  9. Whittemore SR, Ebendal T, LSrkfors L, Olson L, Seiger A, Strcimberg I, Persson H (1986) Developmental and regional expression of nerve grcwth factor messenger RNA and protein in the rat central nervous system. Proc Nat Acad Sci USA 83:817–821

    Article  PubMed  CAS  Google Scholar 

  10. Gage FH, Björklund A, Stenevi U (1984) Denervation releases a neuronal survival factor in adult rat hippocampus. Nature 308:637–639

    Article  PubMed  CAS  Google Scholar 

  11. Korsching S, Auburger G, Heumann R, Scott J, Thoenen H (1985) Levels of nerve growth factor and its mRNA in the central nervous system of the rat correlate with cholinergic innervation. EMBO J 4:1389–1393

    PubMed  CAS  Google Scholar 

  12. Large TH, Bodary SC Clegg DO, Weskamp G, Otten U, Reichardt LF (1986) Nerve growth factor gene expression in the developing rat brain. Science 234:352–355

    Article  PubMed  CAS  Google Scholar 

  13. Gasser UE, Weskamp G, Otten U, Dravid AR (1986) Time course of the elevation of nerve growth factor (NGF) content in the hippocmapus and septum following lesions of the septohippocampal pathway in rats. Brain Res 376:351–356

    Article  PubMed  CAS  Google Scholar 

  14. Lärkfors L, Ebendal T (1987) Highly sensitive enzyme imnunoassays for β-nerve growth factor. J Immunol Meth 97:41–47

    Article  Google Scholar 

  15. Whittemore SR, Lärkfors L, Ebendal T, Holets VR, Ericsson A, Persson H (1987) Increased β-nerve growth factor messenger RNA and protein levels in neonatal rat hippocampus following specific cholinergic lesions. J Neurosci 7:244–251

    PubMed  CAS  Google Scholar 

  16. Schwab ME Otten U, Agid Y, Thoenen H (1979) Nerve growth factor (NGF) in the rat CNS: absence of specific retrograde axonal transport ana tyrosine hydroxylase induction in locus coeruleus and substantia nigra. Brain Res 168:473–483

    Article  PubMed  CAS  Google Scholar 

  17. Seiler M, Schwab ME (1984) Specific retrograde transport of nerve growth factor (NGF) frcm neocortex to nucleus basalis in the rat. Brain Res 300:33–39

    Article  PubMed  CAS  Google Scholar 

  18. Gnahn H, Hefti F, Heumann R, Schwab ME, 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 9:45–52

    Article  CAS  Google Scholar 

  19. Mobley WC, Rutkowski JL, Tennekoan GI, Buchanan K, Johnston MV (1985) Choline acetyltransferase activity in striatum of neonatal rats increased by nerve growth factor, science 229:284–287

    CAS  Google Scholar 

  20. Mobley WC, Rutkowski JL Tennekoan GI, Gemski J, Buchanan K, Johnston MV (1986) Nerve growth factor increases choline acetyl-transferase activity in developing basal forebrain neurons. Mol Brain Res 1:53–62

    Article  Google Scholar 

  21. Hefti F, Dravid A, Hartikka J (1984) Chronic intraventricular injections of nerve growth factor elevate hippocampal choline acetyltransferase activity in adult rats with partial septo hippo- campal lesions. Brain Res 293:305–311

    Article  PubMed  CAS  Google Scholar 

  22. Hefti F (1986) Nerve growth factor promotes survival of septal cholinergic neurons after fimbrial transection. J Neurosci 6:2155–2162

    PubMed  CAS  Google Scholar 

  23. Williams LR, Varon S, Peterson GM, Wictorin K, Fischer W, Björklund A, Gage FH (1986) Infusion of nerve growth factor prevents basal forebrain neuronal death after fimbria fornix transection. Proc Nat Acad Sci USA 83:9231–9235

    Article  PubMed  CAS  Google Scholar 

  24. Kroner LF (1987) Nerve growth factor treatment after brain injury prevents neuronal death. Science 235:214–216

    Article  Google Scholar 

  25. Springer JE, Loy R (1985) Intrahippocarrpal injections of antiserum to nerve growth factor inhibit sympathohippocampal sprouting. Brain Res Bull 15:629–634

    Article  PubMed  CAS  Google Scholar 

  26. Shelton DL, Reichardt LF (1984) Expression of the β-nerve growth factor gene correlates with the density of sympathetic innervaton in effector organs. Proc Nat Acad Sci USA 81:7951–7955

    Article  PubMed  CAS  Google Scholar 

  27. Shelton DL, Reichardt LF (1986) Studies on the expression of the nerve growth factor (NGF) gene in the central nervous system: level and regional distribution of NGF mRNA suggest that NGF functions as a trophic factor for several distinct populations of neurons. Proc Nat Acad Sci USA 83:2714–2718

    Article  PubMed  CAS  Google Scholar 

  28. Goedert M, Fine A, Hunt SP, Ullrich U (1986) Nerve growth factor mRNA in peripheral and central rat tissues and in the human central nervous system: lesion effects in the rat brain and levels in Alzheimer’s disease. Mol Brain Res 1:85–92

    Article  Google Scholar 

  29. Richardson PM, Verge Issa VMK, Riopelle RJ (1986) Distribution of neuronal receptors for nerve qrcwth factor an the rat. J Neurosci 6:2312–2321

    PubMed  CAS  Google Scholar 

  30. Taniuchi M, Schweitzer JB, Johnson EM (1984) Nerve growth factor receptor molecules in rat brain. Proc Nat Acad Sci USA 83:1950–1954

    Article  Google Scholar 

  31. Hefti F, Hartikka J, Salvatierra A, Weiner WJ, Mash DC (1986) Localization of nerve growth factor receptors in cholinergic neurons of the human basal forebrain. Neurosci Lett 69:37–41

    Article  PubMed  CAS  Google Scholar 

  32. Springer JE Koh S, Tayrien MW, Loy R (1987) Basal forebrain maqnocellular neurons stain for nerve growth factor: correlation with cholinergic cell bodies and effects of axotomy. J Neurosci Res (in press)

    Google Scholar 

  33. Johnson EM, Taniuchi M, Clark HB, Springer JE, Koh S, Tayrien MW, Loy R (1987) Demonstration of the retrograde transport of nerve growth factor (NGF) receptor in the peripheral and central nervous system. J Neurosci 7:923–929

    PubMed  CAS  Google Scholar 

  34. Honegger P, Lenoir D (1982) Nerve growth factor (NGF) stimulation of cholinergic telencephalic neurons in aqqreqaticm cell cultures. Dev Brain Res 3:229–238

    Article  CAS  Google Scholar 

  35. Hanegger P (1983) Nerve growth factor-sensitive brain neurons in culture. Mcnogr neural Sci 9:36–42

    Google Scholar 

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

    Article  CAS  Google Scholar 

  37. Hefti F, Hartikka J, Bolger MB (1986) Effect of thyroid hormone analogs on the activity of choline acetyltransferase in cultures of dissociated septal cells. Brain Res 375:413–416

    Article  PubMed  CAS  Google Scholar 

  38. Hatanaka H, Tsukui H (1986) Differential effects of nerve-qrowth factor and glioma-conditioned medium on neurons culturea frcm various reqions of fetal rat central nervous system, Dev Brain Res 30:47–56

    Article  CAS  Google Scholar 

  39. Gähwiler BH, Enz A, Hefti F (1987) Nerve growth factor promotes development of the rat septohippocampal cholinergic projection in vitro. Neurosci Lett 75:6–10

    Article  PubMed  Google Scholar 

  40. Martinez HJ, Dreyfus CF, Miller Jonakait G, Black IB (1985) Nerve growth factor promotes cholinergic development in brain striatal cultures. Proc Nat Acad Sci USA 82:7777–7781

    Article  PubMed  CAS  Google Scholar 

  41. Scott J, Selby M, Urdea M, Quiroga M Bell GI, Rutter WJ (1983) Isolation and nucleotide sequence of a cDNA clone encoding the precursor of mouse nerve growth factor. Nature 302:538–540

    Article  PubMed  CAS  Google Scholar 

  42. Maxam AM, Gilbert W (1977) A new method for sequencing DNA. Proc Nat Acad Sci USA 74:560–564

    Article  PubMed  CAS  Google Scholar 

  43. Chirgwin JM, Priybyla AE, MacDonald RJ, Rutter WJ (1979) Isolation of biologically active ribonucleic acid frcm sources enriched in ribonuclease. Biochem 18:5294–5299

    Article  CAS  Google Scholar 

  44. Aviv H, Leder P (1972) Purification of biologically active globin messenger RNA by chromatography on oligo-thymidylic acid-cellulose. Proc Nat Acad Sci USA 69:1408–1412

    Article  PubMed  CAS  Google Scholar 

  45. Minty AJ, Caravatti M, Benoit K, Cohen A, Daubas P, Weydert A, Gros R, Buckingham ME (1981) Mouse actin messenger RNAs. Construction and characterization of a recaribinant plasmid molecule containing a coTtpementarv transcript of mouse α-actin mRNA, J. Biol Chem 286:1008–1014

    Google Scholar 

  46. Lewis ER, Cotman Qi (1980) Mechanisms of septal lamination in the developing hippocampus revealed by outgrowth of fibers frcrn septal implants. Positional and temporal factors. Brain Res 196:307–330

    Article  PubMed  CAS  Google Scholar 

  47. Cotman CW, Nadler JV (1978) Reactive synaptogenesis in the hippocampus. In: Cotman CW (ed), Neuronal Plasticity, Raven, New York, p 227

    Google Scholar 

  48. Ullrich A, Gray A, Berman C, Dull TJ (1983) Human -nerve growth factor gene sequence highly homologous to that of mouse. Nature 303:821–825

    Article  PubMed  CAS  Google Scholar 

  49. Ebendal T, Larhanmar D, Persson H (1986) Structure and expression of the chicken nerve grcwth factor gene. EMBO J 5:1483–1487

    PubMed  CAS  Google Scholar 

  50. Wion D, Perret C, Frechin N, Keller A, Behar G, Brachet P, Auffray C Molecular cloning of the avian β-nerve growth factor gene: transcription in brain. FEBS Lett 203:82–86

    Article  PubMed  CAS  Google Scholar 

  51. Meier R, Becker-Andre M, Götz R, Heumann R, Shaw A, Thoenen H (1986) Molecular cloning of bovine and chick nerve growth factor (NGF): delineation of conserved and unconserved domains and their relationship to the biological activity and antigenicity of NGF. EMBO J 5:1489–1493

    PubMed  CAS  Google Scholar 

  52. Shaw G, Kamen R (1986) A conserved AU sequence from the 3’ untranslated region of GM-CSF mRNA mediates selective mRNA degredation. Cell 46:559–667

    Article  Google Scholar 

  53. Edwards RH, Selby MJ, Rutter WJ (1986) Differential RNA splicing predicts two distinct nerve growth factor precursors. Nature 319:784–787.

    Article  PubMed  CAS  Google Scholar 

  54. Konkol RJ, Mailman R, Bendeich EG Garrison AM, Mueller RA, Breese GR (1978) Evaluation of the effects of nerve growth factor and antinerve growth factor on the development of central catecholamine- containing neurons. Brain Res 144:277–285

    Article  PubMed  CAS  Google Scholar 

  55. Dreyfus CF, Peterson ER, Grain SM (1980) Failure of nerve growth factor to affect fetal mouse brain stem catecholaminergic neurons in culture. Brain Res 194:540–547

    Article  PubMed  CAS  Google Scholar 

  56. Mesulam M-M, Mufson EJ, Wainer BH, Levey Al (1983) Central cholinergic pathways in the rat: an overview based on an alternative nanenciature (Chl-Ch6). Neurosci 10:1185–1201

    Article  CAS  Google Scholar 

  57. Aghajanian GK, Blocm FE (1967) The formation of synaptic junctions in developing rat brai: a quantitative electron microscopic study. Brain Res 6:716–727

    Article  PubMed  CAS  Google Scholar 

  58. Crain B, Cotman C, Taylor D, Lynch G (1973) A quantitative electron microscopic study of synaptogenesis in the dentate gyrus of the rat. Brain Res 63:195–204

    Article  PubMed  CAS  Google Scholar 

  59. Davies AM, Bandtlcw C, Heumann R, Kbrsching S, Rohrer H, Thoenen H (1987) Timing and site of nerve growth factor synthesis in developing skin in relation to innervation and expression of the receptor. Nature 326:353–358

    Article  PubMed  CAS  Google Scholar 

  60. Matthews DA, Nadler JV, Lynch GSf Cotman CW (1974) Development of cholinergic innervation in the hippocampal formation of the rat. I. Histochemical demonstration of acetylcholinesterase activity. Dev Biol 36:130–141

    Article  PubMed  CAS  Google Scholar 

  61. Milner TA, Lay R, Amaral DG (1983) An anatomical study of the development of the septo-hippocampal projection in the rat. Dev Brain Res 8:343–371

    Article  Google Scholar 

  62. Crutcher KA (1982) Development of the rat septohippocampal Sroiection: a retrograde fluorescent tracer study. Dev Brain Res 3:145–150

    Article  CAS  Google Scholar 

  63. Koh S, Notter MD, Loy R (1986) Nerve growth factor (NGF) promotes cell survival and neurite outgrowth of rat CNS neurons in culture. Correlation with ontogenesis of NGF receptor immunoreactivity. Neurosci Absts 12:1093

    Google Scholar 

  64. Yan Q, Johnson EM (1986) NGF receptor density in developing rats Neurosci Absts 12:1093

    Google Scholar 

  65. Ayer-LeLievre CS, Ebendal T, Olson L, Seiger Å (1983) Localization of nerve growth factor-like unnunoreactivity in rat nervous tissue. Med Biol 61:296–304

    PubMed  CAS  Google Scholar 

  66. Lärkfors L, Ebendal T, Whittemore SR, Persson H, Hoffer B, Olson L Decreased levels of nerve growth factor and its messenger RNA in the aged rat brain. Mol Brain Res (submitted)

    Google Scholar 

  67. Bondareff W (1979) Synaptic atrophy in the senescent hippocampus. Mech Aging Dev 9:163–171

    Article  PubMed  CAS  Google Scholar 

  68. Homberger JC, Buell SJ, Flood DG, McNeill TH, Coleman PD (1985) Stability of numbers but not size of mouse forebrain cholinergic neurons to 53 months. Neurobiol Aging 6:269–275

    Article  Google Scholar 

  69. Collerton D (1986) Cholinergic function and intellectual decline in Alzheiiner’s disease. Neurosci 19:1–28

    Article  CAS  Google Scholar 

  70. Korsching S, Heumann R Thoenen H, Hefti F (1986) Cholinergic denervation of the rat hippocampus by fimbrial transection leads to a transient accumulation of nerve growth factor (NGF) without change in mRNANGF content. Neurosci Lett 66:175–180

    Article  PubMed  CAS  Google Scholar 

  71. Auburger G, Heumann R, Hellweg R, Korsching S, Thoenen H (1987) Developmental changes of nerve growth factor and its mRNA in the rat hippocampus: comparison with choline acetyltransferase. Dev Biol 120:322–328

    Article  PubMed  CAS  Google Scholar 

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© 1988 Springer-Verlag Berlin Heidelberg

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Whittemore, S.R., Persson, H., Ebendal, T., Lärkfors, L., Larhammar, D., Ericsson, A. (1988). Structure and Expression of ß-Nerve Growth Factor in the Rat Central Nervous System. In: Gorio, A., Perez-Polo, J.R., de Vellis, J., Haber, B. (eds) Neural Development and Regeneration. NATO ASI Series, vol 22. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-73148-8_22

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  • DOI: https://doi.org/10.1007/978-3-642-73148-8_22

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