Skip to main content
NCBI home page
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1975 Oct 1;67(1):118–125. doi: 10.1083/jcb.67.1.118

Properties of the beta-nerve growth factor receptor in development

PMCID: PMC2109576  PMID: 1176525

Abstract

The cell surface receptor for beta-nerve growth factor was used as a probe to study the development of embryonic chick sensory ganglia. The ganglia were shown to lose their responsiveness to nerve growth factor in vitro between 14 and 16 days of embryonic age. This loss occurred by a decrease in the magnitude of the maximum biological response, not by a shifting of the response to higher concentrations. Binding assays for the beta-nerve growth factor receptor, using 125I-radiolabelled beta- nerve growth factor, were performed with cells from sensory ganglia 8, 12, 14, 16, 18, and 21 days of age. The assays revealed a twofold increase in the number of receptor sites per ganglion between 8 and 14 days and a sixfold drop between 14 and 16 days of embryonic life. Neither increase nor decrease was accompanied by a large change in the affinity of the receptor for the protein. Together with the results of the bioassay, the data show that the loss of biological responsiveness is correlated with and may be due to a loss of the cells' ability to bind beta-nerve growth factor. Correlation of the results of the binding assays with the known ontogeny of the chick embryo provides a hint at the role of nerve growth factor in normal development.

Full Text

The Full Text of this article is available as a PDF (601.3 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Angeletti R. H., Hermodson M. A., Bradshaw R. A. Amino acid sequences of mouse 2.5S nerve growth factor. II. Isolation and characterization of the thermolytic and peptic peptides and the complete covalent structure. Biochemistry. 1973 Jan 2;12(1):100–115. doi: 10.1021/bi00725a018. [DOI] [PubMed] [Google Scholar]
  2. Angeletti R. H., Mercanti D., Bradshaw R. A. Amino acid sequences of mouse 2.5S nerve growth factor. I. Isolation and characterization of the soluble tryptic and chymotryptic peptides. Biochemistry. 1973 Jan 2;12(1):90–100. doi: 10.1021/bi00725a017. [DOI] [PubMed] [Google Scholar]
  3. BORNSTEIN M. B. Reconstituted rattail collagen used as substrate for tissue cultures on coverslips in Maximow slides and roller tubes. Lab Invest. 1958 Mar-Apr;7(2):134–137. [PubMed] [Google Scholar]
  4. Banerjee S. P., Snyder S. H., Cuatrecasas P., Greene L. A. Binding of nerve growth factor receptor in sympathetic ganglia. Proc Natl Acad Sci U S A. 1973 Sep;70(9):2519–2523. doi: 10.1073/pnas.70.9.2519. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Banks B. E., Banthorpe D. V., Berry A. R., Davies H. S., Doonan S., Lamont D. M., Shipolini R., Vernon C. A. The preparation of nerve growth factors from snake venom. Biochem J. 1968 Jun;108(1):157–158. doi: 10.1042/bj1080157. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Burnham P., Raiborn C., Varon S. Replacement of nerve-growth factor by ganglionic non-neuronal cells for the survival in vitro of dissociated ganglionic neurons. Proc Natl Acad Sci U S A. 1972 Dec;69(12):3556–3560. doi: 10.1073/pnas.69.12.3556. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. EHRMANN R. L., GEY G. O. The growth of cells on a transparent gel of reconstituted rat-tail collagen. J Natl Cancer Inst. 1956 Jun;16(6):1375–1403. [PubMed] [Google Scholar]
  8. Frazier W. A., Boyd L. F., Bradshaw R. A. Interaction of nerve growth factor with surface membranes: biological competence of insolubilized nerve growth factor. Proc Natl Acad Sci U S A. 1973 Oct;70(10):2931–2935. doi: 10.1073/pnas.70.10.2931. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Frazier W. A., Boyd L. F., Bradshaw R. A. Properties of the specific binding of 125I-nerve growth factor to responsive peripheral neurons. J Biol Chem. 1974 Sep 10;249(17):5513–5519. [PubMed] [Google Scholar]
  10. Frazier W. A., Ohlendorf C. E., Boyd L. F., Aloe L., Johnson E. M., Ferrendelli J. A., Bradshaw R. A. Mechanism of action of nerve growth factor and cyclic AMP on neurite outgrowth in embryonic chick sensory ganglia: demonstration of independent pathways of stimulation. Proc Natl Acad Sci U S A. 1973 Aug;70(8):2448–2452. doi: 10.1073/pnas.70.8.2448. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Greene L. A. A dissociated cell culture bioassay for nerve growth factor. Neurobiology. 1974;4(5):286–292. [PubMed] [Google Scholar]
  12. Hendry I. A., Stöckel K., Thoenen H., Iversen L. L. The retrograde axonal transport of nerve growth factor. Brain Res. 1974 Mar 15;68(1):103–121. doi: 10.1016/0006-8993(74)90536-8. [DOI] [PubMed] [Google Scholar]
  13. Herrup K., Shooter E. M. Properties of the beta nerve growth factor receptor of avian dorsal root ganglia. Proc Natl Acad Sci U S A. 1973 Dec;70(12):3884–3888. doi: 10.1073/pnas.70.12.3884. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Herrup K., Stickgold R., Shooter E. M. Trophic functions of the neuron. VI. Other trophic systems. The role of the nerve growth factor in the development of sensory and sympathetic ganglia. Ann N Y Acad Sci. 1974 Mar 22;228(0):381–392. doi: 10.1111/j.1749-6632.1974.tb20527.x. [DOI] [PubMed] [Google Scholar]
  15. Johnson D. G., Silberstein S. D., Hanbauer I., Kopin I. J. The role of nerve growth factor in the ramification of sympathetic nerve fibres into the rat iris in organ culture. J Neurochem. 1972 Sep;19(9):2025–2029. doi: 10.1111/j.1471-4159.1972.tb05112.x. [DOI] [PubMed] [Google Scholar]
  16. Levi-Montalcini R., Angeletti P. U. Nerve growth factor. Physiol Rev. 1968 Jul;48(3):534–569. doi: 10.1152/physrev.1968.48.3.534. [DOI] [PubMed] [Google Scholar]
  17. Oger J., Arnason B. G., Pantazis N., Lehrich J., Young M. Synthesis of nerve growth factor by L and 3T3 cells in culture. Proc Natl Acad Sci U S A. 1974 Apr;71(4):1554–1558. doi: 10.1073/pnas.71.4.1554. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Pannese E., Bianchi R., Calligaris B., Ventura R., Weibel E. R. Quantitative relationships between nerve and satellite cells in spinal ganglia. An electron microscopical study. I. Mammals. Brain Res. 1972 Nov 13;46:215–234. doi: 10.1016/0006-8993(72)90017-0. [DOI] [PubMed] [Google Scholar]
  19. Partlow L. M., Larrabee M. G. Effects of a nerve-growth factor, embryo age and metabolic inhibitors on growth of fibres and on synthesis of ribonucleic acid and protein in embryonic sympathetic ganglia. J Neurochem. 1971 Nov;18(11):2101–2118. doi: 10.1111/j.1471-4159.1971.tb05069.x. [DOI] [PubMed] [Google Scholar]
  20. Smith A. P., Varon S., Shooter E. M. Multiple forms of the nerve growth factor protein and its subunits. Biochemistry. 1968 Sep;7(9):3259–3268. doi: 10.1021/bi00849a032. [DOI] [PubMed] [Google Scholar]
  21. Stoeckel K., Thoenen H. Retrograde axonal transport of nerve growth factor: specificity and biological importance. Brain Res. 1975 Feb 28;85(2):337–341. doi: 10.1016/0006-8993(75)90092-x. [DOI] [PubMed] [Google Scholar]
  22. Varon S., Nomura J., Shooter E. M. The isolation of the mouse nerve growth factor protein in a high molecular weight form. Biochemistry. 1967 Jul;6(7):2202–2209. doi: 10.1021/bi00859a043. [DOI] [PubMed] [Google Scholar]
  23. Varon S., Raiborn C. Dissociation of chick embryo spinal ganglia and the effects on cell yields by the mouse 7S nerve growth factor protein. Neurobiology. 1972;2(3):106–122. [PubMed] [Google Scholar]
  24. Varon S., Raiborn C. Dissociation, fractionation and culture of chick embryo sympathetic ganglionic cells. J Neurocytol. 1972 Oct;1(3):211–221. doi: 10.1007/BF01099934. [DOI] [PubMed] [Google Scholar]
  25. WINICK M., GREENBERG R. E. CHEMICAL CONTROL OF SENSORY GANGLIA DURING A CRITICAL PERIOD OF DEVELOPMENT. Nature. 1965 Jan 9;205:180–181. doi: 10.1038/205180a0. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Cell Biology are provided here courtesy of The Rockefeller University Press

RESOURCES