Abstract
Primary sensory neurones in cranial and dorsal root ganglia (DRG) of adult animals are generally thought to be maintained through connections with their peripheral (but not central) targets by trophic factor(s) other than nerve growth factor (NGF)1. Damage to the peripheral process of sensory neurones results in a dramatic response or even death of the neurones, whereas axotomy (cutting) of the central process does not initiate profound reaction in these neurones. The development and maintenance of neurones are highly dependent on a supply of trophic agents produced by targets and retrogradely transported via the peripheral process to the cell body2. NGF deprivation in fetal rodents produced either by exogenously administered antibodies or by those of maternal origin, results in death of DRG2–5 and of some cranial sensory neurones6. However, as chronic NGF deprivation in neonatal or adult rodents produces little or no cell death7–10, it has been assumed that some other trophic factor(s) derived from the peripheral target sustains sensory neurones in postnatal life. By inducing NGF deprivation by autoimmunizing guinea pigs with mouse NGF and/or by cutting the central root (process) of a DRG, we demonstrate here that under certain conditions DRG neurones require NGF and centrally derived trophic support. Our results indicate that sensory neurones are maintained by the trophic support provided by both peripheral and central targets. This support is mediated by NGF and other as yet unidentified trophic factors. The relative importance of the two target fields and NGF compared with other trophic factors changes during development.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 51 print issues and online access
$199.00 per year
only $3.90 per issue
Rent or buy this article
Prices vary by article type
from$1.95
to$39.95
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Lieberman, A. R. Int. Rev. Neurobiol. 14, 49–124 (1971).
Hamburger, V. & Oppenheim, R. W. Neurosci. Comment. 1, 39–55 (1982).
Gorin, P. D. & Johnson, E. M. Proc. natn. Acad. Sci. U.S.A. 76, 5382–5386 (1979).
Johnson, E. M., Gorin, P. D., Brandeis, L. D. & Pearson, J. Science 210, 916–918 (1980).
Aloe, L., Cozzani, C., Calissano, P. & Levi-Montalcini, R. Nature 291, 413–415 (1981).
Pearson, J., Johnson, E. M. & Brandeis, L. Devl Biol. 96, 32–36 (1983).
Schwartz, J. P., Pearson, J. & Johnson, E. M. Brain Res. 244, 378–381 (1982).
Rich, K. M., Yip, H. K., Osborne, P. A., Schmidt, R. E. & Johnson, E. M. J. comp. Neurol. 230, 110–118 (1984).
Levi-Montalcini, R. & Angeletti, P. U. Physiol. Rev. 48, 534–569 (1968).
Thoenen, H. & Barde, Y. A. Physiol. Rev. 60, 1284–1335 (1980).
Hinsey, J. C., Krupp, M. A. & Lhamon, W T. J. comp. Neurol. 67, 205–214 (1937).
Hare, W. K. & Hinsey, J. C. J. comp. Neurol. 73, 489–502 (1940).
Yip, H. K. & Johnson, E. M. Proc. natn. Acad. Sci. U.S.A. 81, 6245–6249 (1984).
Richardson, P. M. & Riopelle, R. J. J. Neurosci. 4, 1683–1689 (1984).
Coggeshall, R. E. Neurosurgery 4, 443–448 (1979).
Snedecor, G. W. in Statistical Methods (Iowa University Press, 1957).
Konigsmark, B. E. in Contemporary Research Methods in Neuroanatomy (eds Nauta, W. H. & Ebbesson, S. O. E.) 315–340(Springer, New York, 1970).
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Johnson, E., Yip, H. Central nervous system and peripheral nerve growth factor provide trophic support critical to mature sensory neuronal survival. Nature 314, 751–752 (1985). https://doi.org/10.1038/314751a0
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1038/314751a0
This article is cited by
-
A BDNF autocrine loop in adult sensory neurons prevents cell death
Nature (1995)
-
Distribution and characteristics of nerve growth factor binding on cholinergic neurons of rat and monkey forebrain
Neurochemical Research (1987)
-
The nerve growth factor: Thirty-five years later
Bioscience Reports (1987)
-
The nerve growth factor thirty-five years later
In Vitro Cellular & Developmental Biology (1987)
-
Embryonal central neuroepithelial tumors: Current concepts and future challenges
Cancer and Metastasis Reviews (1987)
Comments
By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.