Skip to main content
SpringerLink
Log in

Development of trophic interactions in the vertebrate peripheral nervous system

  • Published:
Molecular Neurobiology Aims and scope Submit manuscript

Abstract

During embryogenesis, the neurons of vertebrate sympathetic and sensory ganglia become dependent on neurotrophic factors, derived from their targets, for survival and maintenance of differentiated functions. Many of these interactions are mediated by the neurotrophins NGF, BDNF, and NT3 and the receptor tyrosine kinases encoded by genes of thetrk family. Both sympathetic and sensory neurons undergo developmental changes in their responsiveness to NGF, the first neurotrophin to be identified and characterized. Subpopulations of sensory neurons do not require NGF for survival, but respond instead to BDNF or NT3 with enhanced survival. In addition to their classic effects on neuron survival, neurotrophins influence the differentiation and proliferation of neural crest-derived neuronal precursors. In both sympathetic and sensory systems, production of neurotrophins by target cells and expression of neurotrophin receptors by neurons are correlated temporally and spatially with innervation patterns. In vitro, embryonic sympathetic neurons require exposure to environmental cues, such as basic FGF and retinoic acid to acquire neurotrophin-responsiveness; in contrast, embryonic sensory neurons acquire neurotrophin-responsiveness on schedule in the absence of these molecules.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Acheson A., Barde Y.-A., and Thoenen H. (1987) High K+-mediated survival of spinal sensory neurons depends on developmental stage.Exp. Cell. Res. 170, 56–63.

    PubMed  CAS  Google Scholar 

  • Aloe L. and Levi-Montalcini R. (1979) Nerve growth factor-induced transformation of immature chromaffin cells in vivo into sympathetic neurons: effect of antiserum to nerve growth factor.Proc. Natl. Acad. Sci. USA 76, 1246–1250.

    PubMed  CAS  Google Scholar 

  • Anderson D. J. (1993) Cell fate determination in the peripheral nervous system: the sympathoadrenal progenitor.J. Neurobiol. 24, 185–198.

    PubMed  CAS  Google Scholar 

  • Anderson D. J. (1988) Cell fate and gene expression in the developing neural crest, inNeural Development and Regeneration, NATO ASI Series, vol. 22 (Gorio A., ed.), Springer-Verlag, Berlin, pp. 188–198.

    Google Scholar 

  • Anderson D. J. and Axel R. (1985) Molecular probes for the development and plasticity of neural crest derivatives.Cell 42, 649–662.

    PubMed  CAS  Google Scholar 

  • Anderson D. J. and Axel R. (1986) A bipotential neuroendocrine precursor whose choice of cell fate is determined by NGF and glucocorticoids.Cell 47, 1079–1090.

    PubMed  CAS  Google Scholar 

  • Angeletti P. U., Levi-Montalcini R., and Caramia F. (1971) Analysis of the effects of the antiserum to the nerve growth factor in adult mice.Brain Res. 27, 343–355.

    PubMed  CAS  Google Scholar 

  • Bandtlow C. E., Heumann R., Schwab M. E., and Thoenen H. (1987) Cellular localization of nerve growth factor synthesis byin situ hybridization.EMBO J. 6, 891–899.

    PubMed  CAS  Google Scholar 

  • Barde, Y.-A. (1989) Trophic factors and neuronal survival.Neuron 2, 1525–1534.

    PubMed  CAS  Google Scholar 

  • Barde Y.-A., Edgar D., and Thoenen H. (1982) Purification of a new neurotrophic factor from mammalian brain.EMBO J. 1, 549–553.

    PubMed  CAS  Google Scholar 

  • Barde Y.-A., Edgar D., and Thoenen H. (1980) Sensory neurons in culture: changing requirements for survival factors during embryonic development.Proc. Natl. Acad. Sci. USA 77, 1199–1203.

    PubMed  CAS  Google Scholar 

  • 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 activatestrk andtrkB.Neuron 7, 857–866.

    PubMed  CAS  Google Scholar 

  • Birren, S. J. and Anderson, D. J. (1990) A v-myc-immortalized sympathoadrenal progenitor cell line in which neuronal differentiation is initiated by FGF but not NGF.Neuron 4, 189–201.

    PubMed  CAS  Google Scholar 

  • Birren S. J., Verdi J. M., and Anderson D. J. (1992) Membrane depolarization induces p140trk and NGF responsiveness, but not p75LNGFR, in MAH cells.Science 257, 395–397.

    PubMed  CAS  Google Scholar 

  • Bothwell M. (1991) Keeping track of neurotrophin receptors.Cell 65, 915–918.

    PubMed  CAS  Google Scholar 

  • Brunso-Bechtold J. and Hamburger H. (1979) Retrograde transport of nerve growth factor in chicken embryo.Proc. Natl. Acad. Sci. USA 76, 1494–1496.

    PubMed  CAS  Google Scholar 

  • Carroll S. L., Silos-Santiago I., Frese S. E., Ruit K. G., Milbrandt J., and Snider W. D. (1992) Dorsal root ganglion neurons expressingtrk are selectively sensitive to NGF deprivationin utero.Neuron 9, 779–788.

    PubMed  CAS  Google Scholar 

  • Chao M. V. (1992) Neurotrophin receptors: a window into neuronal differentiation.Neuron 9, 583–593.

    PubMed  CAS  Google Scholar 

  • Chun L. L. Y. and Patterson P. H. (1977) Role of nerve growth factor in the development of rat sympathetic neuronsin vitro. 1. Survival, growth, and differentiation of catecholamine production.J. Cell. Biol. 75, 694–704.

    PubMed  CAS  Google Scholar 

  • Clegg D. O., Large T. H., Bodary S. C., and Reichardt L. F. (1989) Regulation of nerve growth factor mRNA levels in developing rat heart ventricle is not altered by sympathectomy.Dev. Biol. 134, 30–37.

    PubMed  CAS  Google Scholar 

  • Cohen S. (1960) Purification of a nerve growth-promoting protein from the mouse salivary gland and its neuro-cytotoxic antiserum.Proc. Natl. Acad. Sci. USA 46, 302–311.

    PubMed  CAS  Google Scholar 

  • Cordon-Cardo C., Tapley P., Jing S., Nanduri V., O'Rourke E., Lamballe F., Kovary K., Klein R., Jones K. R., Reichardt L. F., and Barbacid M. (1991) Thetrk tyrosine protein kinase mediates the mitogenic properties of nerve growth factor and neurotrophin-3.Cell 66, 173–183.

    PubMed  CAS  Google Scholar 

  • Coughlin M. D., Boyer D. M., and Black I. B. (1977) Embryologic development of a mouse sympathetic ganglionin vivo andin vitro.Proc. Natl. Acad. Sci. USA 74, 3438–3442.

    PubMed  CAS  Google Scholar 

  • Coughlin M. D., Dibner M. D., Boyer D. M., and Black I. B. (1978) Factors regulating development of an embryonic mouse sympathetic ganglion.Dev. Biol. 66, 513–528.

    PubMed  CAS  Google Scholar 

  • Coughlin M. D. and Collins M. B. (1985) Nerve growth factor-independent development of embryonic mouse sympathetic neurons in dissociated cell culture.Dev. Biol. 110, 392–401.

    PubMed  CAS  Google Scholar 

  • Cowan W. M., Fawcett J. W. O'Leary D. D. M., and Stanfield B. B. (1984) Regressive events in neurogenesis.Science 225, 1258–1265.

    PubMed  CAS  Google Scholar 

  • D'Amico-Martel A., and Noden D. M. (1983) Contributions of placodal and neural crest cells to avian periphel ganglia.Am. J. Anat. 166, 445–468.

    PubMed  Google Scholar 

  • Davies A. M. (1986) The survival and growth of embryonic proprioceptive neurons is promoted by a factor present in skeletal muscle.Dev. Biol. 115, 56–67.

    PubMed  CAS  Google Scholar 

  • Davies A. M. (1987) Molecular and cellular aspects of patterning sensory neurone connections in the vertebrate nervous system.Development 101, 185–208.

    PubMed  CAS  Google Scholar 

  • Davies A. M. (1988) The trigeminal system: an advantageous experimental model for studying neuronal development.Development 103 (Suppl.), 175–183.

    PubMed  Google Scholar 

  • Davies A. M. (1992) Cell death and the trophic requirements of developing sensory neurons, inSensory Neurons: Diversity, Development, and Plasticity (Scott S. A., ed.), Oxford University Press, New York, NY, pp. 194–214.

    Google Scholar 

  • Davies A. and Lumsden A. (1983) Influence of nerve growth factor on developing dorso-medial and ventro lateral neurons of chick and mouse trigeminal ganglia.Int. J. Devel. Neurosci. 1, 171–177.

    Google Scholar 

  • Davies A. and Lumsden A. (1984) Relation of target encounter and neuronal death to nerve growth factor responsiveness in the developing mouse trigeminal ganglion.J. Comp. Neurol. 223, 124–137.

    PubMed  CAS  Google Scholar 

  • Davies A. M. and Lindsay R. M. (1984) Neural, crest-derived spinal and cranial sensory neurones are equally sensitive to NGF but differ in their response to tissue extracts.Dev. Brain Res. 14 121–127.

    CAS  Google Scholar 

  • Davies A. M. and Lindsay R. M. (1985) The cranial sensory ganglia in culture: differences in the response of placode-derived and neural crest-derived neurons to nerve growth factor.Dev. Biol. 111, 62–72.

    CAS  Google Scholar 

  • Davies A. M., Thoenen H., and Barde Y.-A. (1986a) The response of chick sensory neurons to brain-derived neurotrophic factor.J. Neurosci. 6, 1897–1904.

    PubMed  CAS  Google Scholar 

  • Davies A. M., Thoenen H., and Barde Y.-A. (1986b) Different factors from the central nervous system and periphery regulate the survival of sensory neurons.Nature 319, 497–499.

    PubMed  CAS  Google Scholar 

  • Davies A. M., Bandtlow C., Heumann R., Korsching S., Rohrer H., and Thoenen H. (1987a) Timing and site of nerve growth factor synthesis in developing skin in relation to innervation and expression of the receptor.Nature 326, 353–358.

    PubMed  CAS  Google Scholar 

  • Davies A. M., Lumsden A. G. S., and Rohrer H. (1987b) Neural crest-derived proprioceptive neurons express nerve growth factor-receptors but are not supported by nerve growth factor in culture.Neuroscience 1, 37–46.

    Google Scholar 

  • DiStephano P. S., Friedman B., Radziejewski C., Alexander C., Boland P., Schick C. M., Lindsay R., and Weigand S. J. (1992) The neurotrophins BDNF, NT-3, and NGF display distinct patterns of retrograde axonal transport in peripheral and central neurons.Neuron 8, 983–993.

    Google Scholar 

  • Doupe A. J., Landis S. C., and Patterson P. H. (1985) Environmental influences in the development of neural crest derivatives: glucocorticoids, growth factors, and chromaffin cell plasticity.J. Neurosci. 5, 2119–2142.

    PubMed  CAS  Google Scholar 

  • Ebendal T. (1992) Function and evolution in the NGF family and its receptors.J. Neurosci. Res. 32, 461–470.

    PubMed  CAS  Google Scholar 

  • Edgar D., Barde Y.-A., and Thoenen H. (1981) Subpopulations of cultured chick sympathetic neurones differ in their requirements for survival factors.Nature 289, 294–295.

    PubMed  CAS  Google Scholar 

  • Ernsberger U. and Rohrer H. (1988) Neuronal precursor cells in chick dorsal root ganglia: differentiation and survivalin vitro.Dev. Biol. 126, 420–432.

    PubMed  CAS  Google Scholar 

  • Ernsberger U., Edgar D., and Rohrer H. (1989) The survival of early chick sympathetic neurons in vitro is dependent on a suitable substrate but independent of NGF.Dev. Biol. 135, 250–262.

    PubMed  CAS  Google Scholar 

  • Ernfors P., Ibañez C. F., Ebendal T., Olson L., and Persson H. (1990) Molecular cloning and neurotrophic activities of a protein with similarities to nerve growth factor: developmental and topographical expression in the brain.Proc. Natl. Acad. Sci. USA 87, 5454–5458.

    PubMed  CAS  Google Scholar 

  • Godfrey E. W. and Shooter E. M. (1986) Nerve growth factor receptors on chick embryo sympathetic ganglion cells: binding characteristics and development.J. Neurosci. 6, 2543–2550.

    PubMed  CAS  Google Scholar 

  • Goedert M., Otten U., Hunt S. P., Bond A., Chapman D., Schlumpf M., and Lichtensteiger W. (1984) Biochemical and anatomical effects of antibodies against nerve growth factor on developing rat sensory ganglia.Proc. Natl. Acad. Sci. USA 81, 1580–1584

    PubMed  CAS  Google Scholar 

  • Green S. H., Rydel R. E., Connolly J. L., and Greene L. A. (1986) PC12 cell mutants that possess low-but not high-affinity nerve growth factor receptors neither respond to nor internalize nerve growth factor.J. Cell Biol. 102, 830–843.

    PubMed  CAS  Google Scholar 

  • Greene L. A. (1977a) Quantitative studies on the nerve growth factor (NGF) requirement of neurons I. Sympathetic neurons.Dev. Biol. 58, 96–105.

    PubMed  CAS  Google Scholar 

  • Greene L. A. (1977b) Quantitative in vitro studies on the nerve growth factor (NGF) requirement of neurons II. Sensory neurons.Dev. Biol. 58, 106–113.

    PubMed  CAS  Google Scholar 

  • Hallböök F., Ibañez C. F., and Persson H. (1991) Evolutionary studies of the nerve growth factor family reveal a novel member abundantly expressed inXenopus ovary.Neuron 6, 845–858.

    PubMed  Google Scholar 

  • Hamburger V., Brunso-Bechtold J. K., and Yip J. W. (1981) Neuronal death in the spinal ganglia of the chick embryo and its reduction by nerve growth factor.J. Neurosci. 1, 60–71.

    PubMed  CAS  Google Scholar 

  • Hamburger V. and Yip, J. W. (1984) Reduction of experimentally induced neuronal death in spinal ganglia of the chick embryo by nerve growth factor.J. Neurosci. 4, 767–774.

    PubMed  CAS  Google Scholar 

  • Harper S. and Davies A. M. (1990) NGF mRNA expression in developing cutaneous epithelium related to innervation density.Development 110, 515–519.

    PubMed  CAS  Google Scholar 

  • Haskell B. E., Stach R. E., Werrbach-Perez K., and Perez-Polo J. R. (1987) Effect of retinoic acid on nerve growth factor receptors.Cell Tiss Res. 247, 67–73.

    CAS  Google Scholar 

  • Hayashi M., Edgar D., and Thoenen H. (1985) Nerve growth factor changes the relative levels of neuropeptides in developing sensory and sympathetic ganglia of the chick embryo.Dev. Biol. 108, 49–55.

    PubMed  CAS  Google Scholar 

  • Hempstead B. L., Patil N., Olson K., and Chao M. V. (1988) Molecular analysis of the nerve growth factor receptor.Cold Spring Harbor Symp. Quant. Biol. 53, 477–485.

    PubMed  CAS  Google Scholar 

  • Hempstead B. L., Martin-Zanca D., Kaplan D. R., Parada L. F., and Chao M. V. (1991) High-affinity NGF binding requires coexpression of thetrk protooncogene and the low-affinity NGF receptor.Nature 350, 678–683.

    PubMed  CAS  Google Scholar 

  • Hempstead B. L., Rabin S. J., Kaplan L., Reis S., Parada L. F., and Kaplan D. R. (1992) Overexpression of thetrk tyrosine kinase rapidly accelerates nerve growth factor-induced differentiation.Neuron 9, 883–896.

    PubMed  CAS  Google Scholar 

  • Hendry I. A., Stöckel K., Thoenen H., and Iversen L. L. (1974) The retrograde axonal transport of nerve growth factor.Brain Res. 68, 103–121.

    PubMed  CAS  Google Scholar 

  • Hendry I. A. and Campbell J. (1976) Morphometric analysis of rat superior cervical ganglion after axotomy and nerve growth factor treatment.J. Neurocytol. 5, 351–360.

    PubMed  CAS  Google Scholar 

  • Herrup K. and Shooter E. M. (1975) Properties of the B-nerve growth factor receptor in development.J. Cell Biol. 67, 118–125.

    PubMed  CAS  Google Scholar 

  • Heumann R., Korsching S., Scott J., and Thoenen H. (1984) Relationship between levels of nerve growth factor (NGF) and its messenger RNA in sympathetic ganglia and peripheral target tissues.EMBO J. 3, 3183–3189.

    PubMed  CAS  Google Scholar 

  • Hofer M. M. and Barde Y.-A. (1988) Brain-derived neurotrophic factor prevents neuronal deathin vivo.Nature 331, 261–262.

    PubMed  CAS  Google Scholar 

  • Hohn A., Leibrock J., Bailey K., and Barde Y.-A. (1990) Identification and characterization of a novel member of the nerve growth factor/brain-derived neurotrophic factor family.Nature 344, 339–341.

    PubMed  CAS  Google Scholar 

  • Holtzman D. M., Li Y., Parada L. F., Kinsman S., Chen C.-K., Valletta J. S., Zhou J., Long J. B., and Mobley W. C. (1992) p140trk mRNA marks NGF-responsive forebrain neurons: evidence thattrk gene expression is induced by NGF.Neuron 9, 465–478.

    PubMed  CAS  Google Scholar 

  • Honig M. G. and Hume R. I. (1986) Fluorescent carbacyanine dyes allow living neurons of identified origin to be studied in long-term cultures.J. Cell Biol. 103, 171–197.

    PubMed  CAS  Google Scholar 

  • Ip, N. Y., Ibáñez C. F., Nye S. H., McClain J., Jones P. F., Gies D. R., Belluscio L., LeBeau M. M., Espinosa III R., Squinto S. P., Persson H., and Yancopolous G. D. (1992) Mammalian neurotrophin-4: structure, chromosomal location, tissue distribution, and receptor specificity.Proc. Natl. Acad. Sci. USA 89, 3060–3064.

    PubMed  CAS  Google Scholar 

  • Johnson E. M., Andres R. Y., and Bradshaw R. A. (1978) Characterization of the retrograde transport of nerve growth factor (NGF) using high specific activity [125I]NGF.Brain Res. 150, 319–331.

    PubMed  CAS  Google Scholar 

  • Johnson E. M., Gorin P. D., Brandeis L. D., and Pearson J. (1980) Dorsal root ganglion neurons are destroyed by exposurein utero to maternal antibody to nerve growth factor.Science 210, 916–918.

    PubMed  CAS  Google Scholar 

  • Johnson E. M., Rich K. M., and Yip H. K. (1986) The role of NGF in sensory neuronsin vivo.Trends Neurosci. 9, 33–37.

    CAS  Google Scholar 

  • Jones K. R. and Reichardt L. F. (1990) Molecular cloning of the human gene that is a member of the nerve grow factor family.Proc. Natl. Acad. Sci. USA 87, 8060–8064.

    PubMed  CAS  Google Scholar 

  • Kaisho Y., Yashimura K., and Nakahama K. (1990) Cloning and expression of a cDNA encoding a novel human neurotrophic factor.FEBS Lett. 266, 187–191.

    PubMed  CAS  Google Scholar 

  • Kalcheim C., Barde Y.-A., Thoenen H., and LeDouarin N. M. (1987)In vivo effect of brain-derived neurotrophic factor on the survival of developing dorsal root ganglion cells.EMBO J. 6, 2871–2873.

    PubMed  CAS  Google Scholar 

  • Kalcheim C. and Gendreau M. (1988) Brain-derived neurotrophic factor stimulates survival and neuronal differentiation in cultured avian neural crest.Dev. Brain Res. 41, 79–86.

    Google Scholar 

  • Kalcheim C., Carmeli C., and Rosenthal A. (1992) Neurotrophin-3 is a mitogen for cultured neural crest cells.Proc. Natl. Acad. Sci. USA 89, 1661–1665.

    PubMed  CAS  Google Scholar 

  • Kaplan D. R., Hempstead B. L., Martin-Zanca D., Chao M. V., and Parada L. F. (1991a) Thetrk protooncogene product: a signal transducing receptor for nerve growth factor.Science 252, 554–558.

    PubMed  CAS  Google Scholar 

  • Kaplan D. R., Martin-Zanca D., and Parada L. F. (1991b) Tyrosine phosphorylation and tyrosine kinase activity of thetrk proto-oncogene product induced by NGF.Nature 350, 158–160.

    PubMed  CAS  Google Scholar 

  • Katz D. M., Erb M., Lillis R., and Neet K. (1990) Trophic regulation of nodose ganglion cell development.Exp. Neurol. 110, 1–10.

    PubMed  CAS  Google Scholar 

  • Kessler J. A. and Black I. B. (1980) The effects of nerve growth factor (NGF) and antiserum to NGF on the development of embryonic sympathetic neuronsin vivo.Brain Res. 189, 157–168.

    PubMed  CAS  Google Scholar 

  • Klein R., Parada L. F., Coulier F., and Barbacid M. (1989)trkB, a novel tyrosine protein kinase receptor expressed during mouse neural development.EMBO J. 8, 3701–3709.

    PubMed  CAS  Google Scholar 

  • Klein R., Martin-Zanca D., Barbacid M., and Parada L. F. (1990) Expression of the tyrosine kinase receptor genetrkB is confined to the murine embryonic and adult nervous system.Development 109, 845–850.

    PubMed  CAS  Google Scholar 

  • Klein R., Nanduri V., Jing S., Lamballe F., Tapley P., Bryant S., Cordon-Cardo C., Jones K. R., Reichardt L. F., and Barbacid M. (1991) ThetrkB tyrosine protein kinase is a receptor for brain-derived neurotrophic factor and neurotrophin-3.Cell 66, 395–403.

    PubMed  CAS  Google Scholar 

  • Klein R., Lamballe F., Bryant S., and Barbacid M. (1992) ThetrkB tyrosine protein kinase is a receptor for neurotrophin-4.Neuron 8, 947–956.

    PubMed  CAS  Google Scholar 

  • Klingman G. I. (1966)In utero sympathectomy of mice.Int. J. Neuropharmacol. 5, 163–170.

    PubMed  CAS  Google Scholar 

  • Klingman G. I. and Klingman J. D. (1967) Catecholamines in peripheral tissues of mice and cell counts of sympathetic ganglia after the prenatal and postnatal administration of the nerve growth factor antiserum.Int. J. Neuropharmacol. 6, 501–508.

    PubMed  CAS  Google Scholar 

  • Korsching S. and Thoenen H. (1983a) Quantitative demonstration of the retrograde axonal transport of endogenous nerve growth factor.Neurosci. Lett. 39, 1–4.

    PubMed  CAS  Google Scholar 

  • Korsching S. and Thoenen H. (1983b) 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.

    PubMed  CAS  Google Scholar 

  • Korsching S. and Thoenen H. (1987) Two-site enzyme immunoassay for nerve growth factor, inMethods in Enzymology, vol. 147, Academic, Orlando, FL, pp. 167–185.

    Google Scholar 

  • Korsching S. and Thoenen H. (1988) Developmental changes of nerve growth factor levels in sympathetic ganglia and their target organs.Dev. Biol. 126, 40–46.

    PubMed  CAS  Google Scholar 

  • Lahtinen T., Soinila S., and Eranko O. (1986) Agedependent stimulation by atrium explants or nerve growth factor of nerve fibre outgrowth from cocultured embryonic rat sympathetic ganglia.Dev. Brain Res. 27, 51–57.

    CAS  Google Scholar 

  • Lamballe F., Klein R., and Barbacid M. (1991)trkC, a new member of thetrk family of tyrosine protein kinases, is a receptor for neurotrophin-3.Cell 66, 967–979.

    PubMed  CAS  Google Scholar 

  • Larmet Y., Dolphin A. C., and Davies A. M. (1992) Intracellular calcium regulates the survival of early sensory neurons before they become dependent on neurotrophic factors.Neuron 9, 563–574.

    PubMed  CAS  Google Scholar 

  • Lawson S. N. (1992) Morphological and biochemical cell types of sensory neurons, inSensory Neurons: Diversity, Development, and Plasticity, Oxford University Press, New York, NY, pp. 27–59.

    Google Scholar 

  • Leah J. and Kidson C. (1983) Survival of chick embryo sympathetic neurons in cell culture.Int. J. Dev. Neurosci. 1, 403–409.

    Google Scholar 

  • LeDouarin N. M. (1982)The Neural Crest. Cambridge University Press, Cambridge, UK.

    Google Scholar 

  • LeDouarin N. M., Fontaine-Pérus J., and Couly G. (1986) Cephalic ectodermal placodes and neurogenesis.Trends Neurosci. 9, 175–180.

    Google Scholar 

  • Lee K.-F., Li E., Huber J., Landis S. C., Sharpe A. H., Chao M. V., and Jaenisch R. (1992) Targeted mutation of the gene encoding the low affinity NGF receptor p75 leads to deficits in the peripheral sensory nervous system.Cell 69, 737–749.

    PubMed  CAS  Google Scholar 

  • Leibrock J., Lottspeich F., Hohn A., Hofer M., Hengerer B., Masiakowski P., Thoenen H., and Barde Y.-A. (1989) Molecular cloning and expression of brain-derived neurotrophic factor.Nature 341, 149–152.

    PubMed  CAS  Google Scholar 

  • Levi-Montalcini R. (1987) The nerve growth factor: thirty-five years later.EMBO J. 6, 1145–1154.

    PubMed  CAS  Google Scholar 

  • Levi-Montalcini R. and Hamburger V. (1951) Selective growth-stimulating effects of mouse sarcoma on the sensory and sympathetic nervous system of the chick embryo.J. Exp. Zool. 116, 321–362.

    PubMed  CAS  Google Scholar 

  • Levi-Montalcini R. and Booker B. (1960) Destruction of the sympathetic ganglia in mammals by an antiserum to a nerve-growth protein.Proc. Natl. Acad. Sci. USA 46, 384–391.

    PubMed  CAS  Google Scholar 

  • Levi-Montalcini R. and Angeletti P. U. (1963) Essential role of the nerve growth factor in the survival and maintenance of dissociated sensory and sympathetic embryonic nerve cellsin vitro.Dev. Biol. 7, 653–659.

    PubMed  CAS  Google Scholar 

  • Levi-Montalcini R. and Angeletti P. U. (1968) Nerve growth factor.Physiol. Rev. 48, 534–569.

    PubMed  CAS  Google Scholar 

  • Lillien L. E. and Claude P. (1985) Nerve growth factor is a mitogen for cultured chromaffin cells.Nature 317, 632–634.

    PubMed  CAS  Google Scholar 

  • Lindsay R. M. (1992) The role of neurotrophic factors in the functional maintenance of mature sensory neurons, inSensory Neurons: Diversity, Development, and Plasticity (Scott S. A., ed.), Oxford University Press, New York, NY, pp. 404–420.

    Google Scholar 

  • Lindsay R. M. and Tarbit J. (1979) Developmentally regulated induction of neurite outgrowth from immature chick sensory neurons (DRG) by homogenates of avian or mammalian heart, liver, and brain.Neurosci. Lett. 12, 195–200.

    PubMed  CAS  Google Scholar 

  • Lindsay R. M. and Peters C. (1984) Spinal cord contains neurotrophic activity for spinal nerve sensory neurons. Late developmental appearance of a survival factor distinct from nerve growth factor.Neuroscience 12, 45–51.

    PubMed  CAS  Google Scholar 

  • Lindsay R. M. and Rohrer H. (1985) Placodal sensory neurons in culture: nodose ganglion neurons are unresponsive to NGF, lack NGF receptors but are supported by a liver-derived neurotrophic factor.Dev. Biol. 112, 30–48.

    PubMed  CAS  Google Scholar 

  • Lindsay R. M., Thoenen H., and Barde Y.-A. (1985) Placode-and neural crest-derived sensory neurons are responsive at early developmental stages to brain-derived neurotrophic factor.Dev. Biol. 112, 319–328.

    PubMed  CAS  Google Scholar 

  • Loeb D. M., Maragos J., Martin-Zanca D., Chao M., Parada L. F., and Greene L. A. (1991) Thetrk proto-oncogene rescues NGF responsiveness in mutant NGF-nonresponsive PC12 cell lines.Cell 66, 961–966.

    PubMed  CAS  Google Scholar 

  • Ludueña M. A. (1973) Nerve cell differentiationin vitro.Dev. Biol. 33, 268–284.

    PubMed  Google Scholar 

  • Maisonpierre P. C., Belluscio L., Squinto S., Ip N. Y., Furth M. E., Lindsay R. M., and Yancopoulos G. D. (1990) Neurotrophin-3: a neurotrophic factor related to NGF and BDNF.Science 247, 1446–1451.

    PubMed  CAS  Google Scholar 

  • Martin-Zanca D., Barbacid M., and Parada L. F. (1990) Expression of thetrk proto-oncogene is restricted to the sensory cranial and spinal ganglia of neural crest origin in mouse development.Genes Dev. 4, 683–694.

    PubMed  CAS  Google Scholar 

  • Marusich M. F., Pourmehr K. P., and Weston J. A. (1986) A monoclonal antibody (SNI) identifies a subpopulation of avian sensory neurons whose distribution is correlated with axial level.Dev. Biol. 118, 494–504.

    PubMed  CAS  Google Scholar 

  • Meakin S. O., Suter U., Drinkwater C. C., Welcher A. A., and Shooter E. M. (1992) The rattrk protooncogene exhibits properties characteristic of the slow NGF receptor.Proc. Natl. Acad. Sci. USA 89, 2374–2378.

    PubMed  CAS  Google Scholar 

  • Naujoks K. W., Korsching S., Rohrer H., and Thoenen H. (1982) Nerve growth factor-mediated induction of tyrosine hydroxylase and of neurite outgrowth in cultures of bovine adrenal cells: dependence on developmental stage.Dev. Biol. 92, 365–379.

    PubMed  CAS  Google Scholar 

  • Noden D. M. (1993) Spatial integration among cells forming the cranial peripheral nervous system.J. Neurobiol. 24, 248–261.

    PubMed  CAS  Google Scholar 

  • Oppenheim R. W. (1985) Naturally occurring cell death during neural development.Trends Neurosci. 8, 487–493.

    Google Scholar 

  • Oppenheim R. W., Maderdrut J. L., and Wells D. J. (1982) Cell death of motoneurons in the chick embryo spinal cord. VI. Reduction of naturally occurring cell death in the thoracolumbar column of Terni by nerve growth factor.J. Comp. Neurol. 210, 174–189.

    PubMed  CAS  Google Scholar 

  • Otten U., Goedert M., Schwab M., and Thibault J. (1979) Immunization of adult rats against 2.5S NGF: effects on the peripheral sympathetic nervous system.Brain Res. 176, 79–90.

    PubMed  CAS  Google Scholar 

  • Partlow L. M. and Larrabee M. G. (1971) Effects of a nerve growth factor, embryonic age and metabolic inhibitors on synthesis of ribonucleic acid and protein in embryonic sensory ganglia.J. Neurochem. 18, 2101–2118.

    PubMed  CAS  Google Scholar 

  • Pearson J., Johnson E. M., and Brandeis L. (1983) Effects of antibodies to nerve growth factor on intrauterine development of derivatives of cranial neural crest and placode in the guinea pig.Dev. Biol. 96, 32–36.

    PubMed  CAS  Google Scholar 

  • Purves D. (1988)Body and Brain. A Trophic Theory of Neuronal Connections. Harvard University Press, Cambridge, MA.

    Google Scholar 

  • Rich K. M., Yip H. K., Osborne P. A., Schmidt R. E., and Johnson E. M. (1984) Role of nerve growth factor in the adult dorsal root ganglia neuron and its response to injury.J. Comp. Neurol. 230, 110–118.

    PubMed  CAS  Google Scholar 

  • Richardson P. M. and Riopelle R. J. (1984) Uptake of nerve growth factor along peripheral and spinal axons of primary sensory neurons.J. Neuroscience 4, 1683–1689.

    CAS  Google Scholar 

  • Ritter A. M., Lewin G. R., Krema N. E., and Mendell L. M. (1991) Requirement for nerve growth factor in the development of myelinated nociceptorsin vivo.Nature 350, 500–502.

    PubMed  CAS  Google Scholar 

  • Rodriguez-Tébar A., Dechant G., and Barde Y.-A. (1990) Binding of brain-derived neurotrophic factor to the nerve growth factor receptor.Neuron 4, 487–492.

    PubMed  Google Scholar 

  • Rodriguez-Tébar A. and Rohrer H. (1991) Retinoic acid induces NGF-dependent survival response and high-affinity NGF receptors in immature chick sympathetic neurons.Development 112, 813–820.

    PubMed  Google Scholar 

  • Rodriguez-Tébar A., Dechant G., Götz R., and Barde Y.-A. (1992) Binding of neurotrophin-3 to its neuronal receptors and interactions with nerve growth factor and brain-derived neurotrophic factor.EMBO J. 11, 917–922.

    PubMed  Google Scholar 

  • Rohrer H. and Barde Y.-A. (1982) Presence and disappearance of nerve growth factor receptors on sensory neurons in culture.Dev. Biol. 89, 309–315.

    PubMed  CAS  Google Scholar 

  • Rohrer H., Thoenen H., and Edgar D. (1983) Presence of nerve growth factor receptors and catecholamine uptake in subpopulations of chick sympathetic neurons: correlation with survival factor requirements in culture.Dev. Biol. 99, 34–40.

    PubMed  CAS  Google Scholar 

  • Rohrer H., Hofer M., Hellweg R., Korsching S., Stehle A. D., Saadat S., and Thoenen H. (1988a) Antibodies against mouse nerve growth factor interfere in vivo with the development of avian sensory and sympathetic neurones.Development 103, 545–552.

    PubMed  CAS  Google Scholar 

  • Rohrer H., Heumann R., and Thoenen H. (1988b) The synthesis of nerve growth factor (NGF) in developing skin is independent of innervation.Dev. Biol. 128, 240–244.

    PubMed  CAS  Google Scholar 

  • Rosenthal A., Goeddel D. V., Nguyen T., Lewis M., Shih A., Laramee G. R., Nikolics K., and Winslow J. W. (1990) Primary structure and biological activity of a novel human neurotrophic factor.Neuron 4, 767–773.

    PubMed  CAS  Google Scholar 

  • Ross A. H. (1991) Identification of tyrosine kinasetrk as a nerve growth factor receptor.Cell Regul. 2, 685–690.

    PubMed  CAS  Google Scholar 

  • Rubin E. (1985a) Development of the rat superior cervical ganglion: ganglion cell maturation.J. Neurosci. 5, 673–684.

    PubMed  CAS  Google Scholar 

  • Rubin E. (1985b) Development of the rat superior cervical ganglion: ingrowth of preganglionic axons.J. Neurosci. 5, 685–696.

    PubMed  CAS  Google Scholar 

  • Ruit K. G., Elliott J. L., Osborne P. A., Yan Q., and Snider W. D. (1992) Selective dependence of mammalian dorsal root ganglion neurons on nerve growth factor during embryonic development.Neuron 8, 573–587.

    PubMed  CAS  Google Scholar 

  • Schecterson L. C. and Bothwell M. (1992) Novel roles for neurotrophins are suggested by BDNF and NT3 mRNA expression in developing neurons.Neuron 9, 449–463.

    PubMed  CAS  Google Scholar 

  • Shelton D. L. and Reichardt L. F. (1984) Expression of the B-nerve growth factor gene correlates with the density of sympathetic innervation in effector organs.Proc. Natl. Acad. Sci. USA 81, 7951–7955.

    PubMed  CAS  Google Scholar 

  • Shelton D. L. and Reichardt L. F. (1986) Studies on the regulation of B nerve growth factor gene expression in iris: the level of mRNA encoding nerve growth factor is increased in iris in explant culturesin vitro, but not in irises deprived of sensory or sympathetic innervationin vivo.J. Cell Biol. 102, 1940–1948.

    PubMed  CAS  Google Scholar 

  • Sieber-Blum M. (1991) Role of the neurotrophic factors BDNF and NGF in the commitment of pluripotent neural crest cells.Neuron 6, 949–955.

    PubMed  CAS  Google Scholar 

  • Soppet D., Escandon E., Maragos J., Middlemas D. S., Reid S. W., Blair J., Burton L. E., Stanton B. R., Kaplan D. R., Hunter T., Nikolics K., and Parada L. F. (1991) The neurotrophic factors brain-derived neurotrophic factor and neurotrophin-3 are ligands for thetrkB tyrosine kinase receptor.Cell 65, 895–903.

    PubMed  CAS  Google Scholar 

  • Squinto S. P., Stitt T. N., Aldrich T. H., Davis S., Bianco S. M., Radziejewski C., Glass D. J., Masiakowski P., Furth M. E., Valenzuela D. M., DiStephano P. S., and Yancopolous G. D. (1991)trkB encodes a functional receptor for brain-derived neurotrophic factor and neurotrophin-3 but not nerve growth factor.Cell 65, 885–893.

    PubMed  CAS  Google Scholar 

  • Stemple D. L., Mahanthappa N. K., and Anderson D. J. (1988) Basic FGF induces neuronal differentiation, cell division, and NGF dependence in chromaffin cells: a sequence of events in sympathetic development.Neuron 1, 517–525.

    PubMed  CAS  Google Scholar 

  • Stöckel K. and Thoenen H. (1975) Retrograde axonal transport of nerve growth factor: specificity and biological importance.Brain Res. 85, 337–341.

    Google Scholar 

  • Sutter A., Riopelle R. J., Harris-Warrick R. M., and Shooter E. M. (1979) Nerve growth factor receptors: characterization of two distinct binding sites on chick embryo sensory ganglia cells.J. Biol. Chem. 254, 5972–5982.

    PubMed  CAS  Google Scholar 

  • Thoenen H. and Barde Y.-A. (1980) Physiology of nerve growth factor.Physiol. Rev. 60, 1284–1335.

    PubMed  CAS  Google Scholar 

  • Tosney K. W. (1982) The segregation and early migration of cranial neural crest cells in the avian embryo.Dev. Biol. 89, 13–24.

    PubMed  CAS  Google Scholar 

  • Unsicker K., Krisch B., Otten U., and Thoenen H. (1978) Nerve growth factor-induced fiber out-growth from isolated rat adrenal chromaffin cells: impairment by glucocorticoids.Proc. Natl. Acad. Sci. USA 75, 3498–3502.

    PubMed  CAS  Google Scholar 

  • Vogel K. S. and Weston J. A. (1990a) The sympathoadrenal lineage in avian embryos I. Adrenal chromaffin cells lose neuronal traits during embryogenesis.Dev. Biol. 139, 1–12.

    PubMed  CAS  Google Scholar 

  • Vogel K. S. and Weston J. A. (1990b) The sympathoadrenal lineage in avian embryos II. Effects of glucocorticoids on cultured neural crest cells.Dev. Biol. 139, 13–23.

    PubMed  CAS  Google Scholar 

  • Vogel K. S. and Davies A. M. (1991) The duration of neurotrophic factor independence in early sensory neurons is matched to the time course of target field innervation.Neuron 7, 819–830.

    PubMed  CAS  Google Scholar 

  • Vogel K. S. (1992) Origins and early development of vertebrate cranial sensory neurons, inSensory Neurons: Diversity, Development, and Plasticity (Scott S. A., ed.), Oxford University Press, New York, NY, pp. 171–193.

    Google Scholar 

  • Weis J. S. (1968) Analysis of the development of the nervous system of the zebrafish,Brachydanio rerio II. The effect of nerve growth factor and its antiserum on the nervous system of the zebrafish.J. Embryol. Exp. Morphol. 19, 121–135.

    PubMed  CAS  Google Scholar 

  • Weskamp G. and Reichardt L. F. (1991) Evidence that biological activity of NGF is mediated through a novel subclass of high affinity receptors.Neuron 6, 649–663.

    PubMed  CAS  Google Scholar 

  • Weston J. A. (1970) The migration and differentiation of neural crest cells.Adv. Morphogen. 8, 41–114.

    CAS  Google Scholar 

  • Weston J. A. (1991) The sequential segregation and fate of developmentally-restricted intermediate cell populations in the neural crest lineage.Curr. Top. Dev. Biol. 25, 133–153.

    PubMed  CAS  Google Scholar 

  • Wright E. M., Vogel K. S., and Davies A. M. (1992) Neurotrophic factors promote the maturation of developing sensory neurons before they become dependent on these factors for survival.Neuron 9, 139–150.

    PubMed  CAS  Google Scholar 

  • Wyatt S., Shooter E. M., and Davies A. M. (1990) Expression of the NGF receptor gene in sensory neurons and their cutaneous targets prior to and during innervation.Neuron 2, 421–427.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Molecular Embryology Section; NCl-Frederick Cancer Research and Development Center, ABL-Basic Research Program, 21702-1201, Frederick, MD

    Kristine S. Vogel

Authors
  1. Kristine S. Vogel
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Vogel, K.S. Development of trophic interactions in the vertebrate peripheral nervous system. Mol Neurobiol 7, 363–382 (1993). https://doi.org/10.1007/BF02769183

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02769183

Index Entries

Search

Navigation