Abstract
The importance of Nerve Growth Factor (NGF) for the development and the maintenance of differentiated properties of peripheral sympathetic and neural crest- derived sensory neurons as well as for basal forebrain cholinergic neurons is well established (cf Levi-Montalcini & Angeletti, 1968; Greene & Shooter, 1980; Thoenen & Barde, 1980; Thoenen et al. 1987). NGF interacts with specific neuronal receptors, is internalized and is subsequently retrogradely transported to the perikaryon. During the last few years new methodological approaches allowed the direct analysis of the retrograde messenger function of NGF between target organs and corresponding NGF-responsive neurons. In the adult animal it was demonstrated that the density of sympathetic innervation is correlated with the levels of NGF (Korsching & Thoenen 1983) and mRNANGF (Heumann et al. 1984, Shelton & Reichardt 1984). Thus, the ratio between NGF and mRNANGF in various target tissues of sympathetic or sensory neurons is relatively constant. However, in sympathetic and sensory ganglia containing the cell bodies of NGF-responsive neurons the levels of NGF are (relatively) very high whereas the mRNANGF levels are at the detection limit (Heumann et al. 1984, Davies et al. 1987a). Similarly, in the sciatic nerve (Heumann et al. 1987a) the ratio between NGF and mRNANFG is up to 100–fold higher than in peripheral target tissues of sympathetic and sensory neurons, reflecting the very low contribution of local synthesis to the sciatic NGF content. This is in agreement with the observation that after ligation of the sciatic nerve NGF accumulates distally to the ligature whereas proximaily NGF levels are reduced to the detection limit of the NGF assay (Korsching and Thoenen, 1983b). The importance of the NGF supply from the peripheral target tissues is also demonstrated by the fact that destruction of sympathetic nerve terminals by 6–OH- dopamine results in a rapid decay of NGF levels in the sympathetic ganglia (t1/2 = 4-5 hours) (Korsching and Thoenen, 1985) with a concomitant increase of NGF in the corresponding peripheral target organs.
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References
Abercrombie M Johnson ML (1946) Quantitative histology of Wallerian degeneration I. Nuclear population in rabbit sciatic nerve. J Anatomy 80:37–50
Bandtlow CE, Heumann R, Schwab ME, Thoenen H (1987) Cellular localization of nerve growth factor synthesis by in situ-hybridization. EMBO J 6:69–91
Beuche W, Friede RL (1986) Myelin phagocytosis in Wallerian degeneration of peripheral nerves depends on silica-sensitive, bg/bg-negative and Fc-positive monocytes. Brain Res 378:97–106
Cajal RY (1928) Degeneration of the peripheral stump. In: May RM (ed and transl) Degeneration and Regeneration of the Nervous System. University Press, Oxford, vol 1, pp 100–126
Davies AM, Bandtlow C, Heumann R, Korsching S, Rohrer H, Thoenen H (1987a) The site and timing of nerve growth factor (NGF) synthesis in developing skin in relation to its innervation by sensory neurones and their expression of NGF receptors. Nature 326:353–358
Greene LA, Shooter EM (1980) The nerve growth factor: biochemistry, synthesis, and mechanism of action. Ann Rev Neurosci 3:353–402
Hallpike JF, Adams CWM, Bayiiss OB (1970) Histochemistry of myelin. IX. Neutral and acid proteinases in early Wallerian degeneration. Histochem J 2:209–218
Heumann R, Korsching S, Scott J, Thoenen H (1984a) Relationship between levels of nerve growth factor (NGF) and its messenger RNA in sympathetic ganglia and peripheral target tissues. EMBO J 3:3183–3189
Heumann R, Thoenen H (1986) Comparison between the time course of changes in nerve growth factor (NGF) protein levels and those of its messenger RNA in the cultured rat iris. J Biol Chem 261:9246–9249
Heumann R, Korsching S, Bandtlow C, Thoenen H (1987a) Changes of nerve growth factor synthesis in non-neuronal cells in response to sciatic nerve transection. J Ceil Biol 104:1623–1631
Heumann R, Lindholm D, Bandtlow C, Meyer M, Radeke MJ, Misko TP, Shooter E, Thoenen H (1987b) Differential regulation of nerve growth factor (NGF) and NGF- receptor mRNA in the rat sciatic nerve during development, degeneration and regeneration; role played by macrophages. Proc Natl Acad Sci USA, in press
Johnson EM, Taniuchi M, Clark HB, Springer JE, Koh S, Tayrien MW, Loy R (1987a) Demonstration of the retrograde transport of nerve growth factor receptor in the peripheral and central nervous system. J Neurosci 7:923–929
Korsching S, Thoenen H (1983a) Nerve growth factor in sympathetic ganglia and corresponding target organs of the rat: correlation with density of sympathetic innervation Proc Natl Acad Sci USA 80:3513–3516
Korsching S, Thoenen H (1983b) Quantitative demonstration of the retrograde axonal transport of endogenous nerve growth factor. Neurosci Lett 39:1–4
Korsching S, Thoenen H (1985) Treatment with 6–hydroxydopamine and colchicine decreases nerve growth factor levels in sympathetic ganglia and increases them in the corresponding target tissues. J Neurosci 5:1058–1061
Levi-Montalcini R (1987) The nerve growth factor: thirty-five years later. EMBO J 6:1145–1154
Lumsden AGS, Davies AM (1983) Earliest sensory nerve fibres are guided to peripheral targets by attractants other than nerve growth factor. Nature 306:786–788
Müller HW, Gebicke-Harter PJ, Hangen DH, Shooter EM (1985) A specific 37,000- dalton protein that accumulates in regenerating but not in nonregenerating mammalian nerves. Science 228:499–501
Perry VH, Brown MC, Gordon S (1987) The macrophage response to central and peripheral nerve injury. J Exp Med 165:1218–1223
Purves D, Lichtman JW (1985) Principles of neural development. Sinauer Associates, Inc, Sunderland, MA, pp 131–178
Radeke MJ, Misko TP, Hsu C, Herzenberg LA, Shooter EM (1987) Gene transfer and molecular cloning of the rat nerve growth factor receptor: a new class of receptors. Nature 325:593–597
Rich KM, Luszczynski JR, Osborne PA, Johnson EM (1987) Nerve growth factor protects adult sensory neurons from cell death and atrophy caused by nerve injury. J Neurocytol 16:261–268
Rohrer H (1985) Nonneuronal cells from chick sympathetic and dorsal root sensory ganglia express catecholamine uptake and receptors for nerve growth factor during development. Dev Biol 111:95–107
Salzer JL, Bunge RP (1980) Studies on Schwann cell proliferation. I. An analysis in tissue culture of proliferation during development, Wallerian degeneration, and direct injury. J Cell Biol 84:739–752
Scheidt P, Waehneldt TV, Beuche W, Friede RL (1986) Changes of myelin proteins during Wallerian degeneration in situ and in millipore diffusion chambers preventing active phagocytosis. Brain Res 379:380–384
Seilheimer B, Schachner M (1987) Regulation of neural cell adhesion molecule expression on cultured mouse Schwann cells by nerve growth factor. EMBO J 6:1611–1616
Shelton DL, Reichardt LF (1984) Expression of the nerve growth factor gene correlates with the density of sympathetic innervation in effector organs. Proc Natl Acad Sci USA 81:7951–7955
Stoll G, Muller HW (1986) Macrophages in the peripheral nervous system and astroglia in the central nervous system of rat commonly express apolipoprotein E during development but differ in their response to injury. Neurosci Lett 72:233–238
Taniuchi M, Clark HB, Johnson Jr EM (1986) Induction of nerve growth factor receptor in Schwann cells after axotomy. Proc Natl Acad Sci USA 83:4094–4098
Thoenen H, Barde Y-A (1980) Physiology of nerve growth factor. Physiol Rev 60:1284–1335
Thoenen H, Bandtlow C, 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
Unanue ER, Alien PM (1987) The basis for the immunoregulatory role of macrophages and other accessory cells. Science 236:551–557
Webster HdeF, Martin JR, O’Connell MF (1973) The relationships between interphase Schwann cells and axons before myelination: A quantitative electron microscopic study. Dev Biol 32:401–416
Zimmermann A, Sutter A (1983) B-nerve growth factor (B-NGF) receptors on glial-cells - cell-cell interaction between neurons and Schwann-cells in cultures of chick sensory ganglia. EMBO J 2:879–885
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© 1988 Springer-Verlag Berlin Heidelberg
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Heumann, R. et al. (1988). Regulation of the Synthesis of Nerve Growth Factor and Nerve Growth Factor Receptor. 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_24
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