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. 1983 Apr;80(7):2091–2094. doi: 10.1073/pnas.80.7.2091

An effect of nerve growth factor on parasympathetic neurite outgrowth.

F Collins, A Dawson
PMCID: PMC393759  PMID: 6340114

Abstract

Addition of nerve growth factor (NGF) to dissociated parasympathetic ciliary ganglion neurons resulted, within 60 min of its addition, in a 2-fold increase in average neurite length and an accompanying enlargement and spreading of neuronal growth cones. These effects occurred over a concentration range of NGF of 0.1-10 ng/ml and were blocked by affinity-purified antibody to NGF. Epidermal growth factor, fibroblast growth factor, and angiotensin did not have these effects, although insulin at high concentrations was able to induce a response similar to that of NGF. Dissociated sympathetic chain neurons also responded to NGF with increased neurite lengths, and, in addition, NGF considerably extended the survival time of these neurons in culture. However, the effect of NGF on ciliary ganglion neurons was limited to neurite outgrowth, and NGF did not promote the survival of these parasympathetic neurons.

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Selected References

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  1. Adler R., Varon S. Cholinergic neuronotrophic factors: V. Segregation of survival- and neurite-promoting activities in heart-conditioned media. Brain Res. 1980 Apr 28;188(2):437–448. doi: 10.1016/0006-8993(80)90043-8. [DOI] [PubMed] [Google Scholar]
  2. Avrith D. B., Lewis M. E., Fitzsimons J. T. Renin-like effects of NGF evaluated using renin-angiotensin antagonists. Nature. 1980 May 22;285(5762):248–250. doi: 10.1038/285248a0. [DOI] [PubMed] [Google Scholar]
  3. Bradshaw R. A. Nerve growth factor. Annu Rev Biochem. 1978;47:191–216. doi: 10.1146/annurev.bi.47.070178.001203. [DOI] [PubMed] [Google Scholar]
  4. Campenot R. B. Local control of neurite development by nerve growth factor. Proc Natl Acad Sci U S A. 1977 Oct;74(10):4516–4519. doi: 10.1073/pnas.74.10.4516. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Collins F. Axon initiation by ciliary neurons in culture. Dev Biol. 1978 Jul;65(1):50–57. doi: 10.1016/0012-1606(78)90178-1. [DOI] [PubMed] [Google Scholar]
  6. Collins F., Dawson A. Conditioned medium increases the rate of neurite elongation: separation of this activity from the substratum-bound inducer of neurite outgrowth. J Neurosci. 1982 Aug;2(8):1005–1010. doi: 10.1523/JNEUROSCI.02-08-01005.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Collins F., Garrett J. E., Jr Elongating nerve fibers are guided by a pathway of material released from embryonic nonneuronal cells. Proc Natl Acad Sci U S A. 1980 Oct;77(10):6226–6228. doi: 10.1073/pnas.77.10.6226. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Collins F. Induction of neurite outgrowth by a conditioned-medium factor bound to the culture substratum. Proc Natl Acad Sci U S A. 1978 Oct;75(10):5210–5213. doi: 10.1073/pnas.75.10.5210. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Coughlin M. D. Target organ stimulation of parasympathetic nerve growth in the developing mouse submandibular gland. Dev Biol. 1975 Mar;43(1):140–158. doi: 10.1016/0012-1606(75)90137-2. [DOI] [PubMed] [Google Scholar]
  10. Crutcher K. A., Collins F. In vitro Evidence for two distinct hippocampal growth factors: basis of neuronal plasticity? Science. 1982 Jul 2;217(4554):67–68. doi: 10.1126/science.7089542. [DOI] [PubMed] [Google Scholar]
  11. Ebendal T., Jacobson C. O. Tests of possible role of NGF in neurite outgrowth stimulation exerted by glial cells and heart explants in culture. Brain Res. 1977 Aug 12;131(2):373–378. doi: 10.1016/0006-8993(77)90531-5. [DOI] [PubMed] [Google Scholar]
  12. Frazier W. A., Angeletti R. H., Bradshaw R. A. Nerve growth factor and insulin. Science. 1972 May 5;176(4034):482–488. doi: 10.1126/science.176.4034.482. [DOI] [PubMed] [Google Scholar]
  13. Greene L. A. Quantitative in vitro studies on the nerve growth factor (NGF) requirement of neurons. I. Sympathetic neurons. Dev Biol. 1977 Jul 1;58(1):96–105. doi: 10.1016/0012-1606(77)90076-8. [DOI] [PubMed] [Google Scholar]
  14. Greene L. A. Quantitative in vitro studies on the nerve growth factor (NGF) requirement of neurons. II. Sensory neurons. Dev Biol. 1977 Jul 1;58(1):106–113. doi: 10.1016/0012-1606(77)90077-x. [DOI] [PubMed] [Google Scholar]
  15. Greene L. A., Shooter E. M. The nerve growth factor: biochemistry, synthesis, and mechanism of action. Annu Rev Neurosci. 1980;3:353–402. doi: 10.1146/annurev.ne.03.030180.002033. [DOI] [PubMed] [Google Scholar]
  16. Greene L. A., Tischler A. S. Establishment of a noradrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor. Proc Natl Acad Sci U S A. 1976 Jul;73(7):2424–2428. doi: 10.1073/pnas.73.7.2424. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Guroff G., Montgomery P., Tolson N., Lewis M. E., End D. Induction of ornithine decarboxylase by renin-free nerve growth factor. Proc Natl Acad Sci U S A. 1980 Aug;77(8):4607–4609. doi: 10.1073/pnas.77.8.4607. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Helfand S. L., Riopelle R. J., Wessells N. K. Non-equivalence of conditioned medium and nerve growth factor for sympathetic, parasympathetic, and sensory neurons. Exp Cell Res. 1978 Apr;113(1):39–45. doi: 10.1016/0014-4827(78)90085-x. [DOI] [PubMed] [Google Scholar]
  19. Helfand S. L., Smith G. A., Wessells N. K. Survival and development in culture of dissociated parasympathetic neurons from ciliary ganglia. Dev Biol. 1976 Jun;50(2):541–547. doi: 10.1016/0012-1606(76)90174-3. [DOI] [PubMed] [Google Scholar]
  20. LEVI-MONTALCINI R., ANGELETTI P. U. Essential role of the nerve growth factor in the survival and maintenance of dissociated sensory and sympathetic embryonic nerve cells in vitro. Dev Biol. 1963 Mar;6:653–659. doi: 10.1016/0012-1606(63)90149-0. [DOI] [PubMed] [Google Scholar]
  21. Max S. R., Schwab M., Dumas M., Thoenen H. Retrograde axonal transport of nerve growth factor in the ciliary ganglion of the chick and the rat. Brain Res. 1978 Dec 29;159(2):411–415. doi: 10.1016/0006-8993(78)90549-8. [DOI] [PubMed] [Google Scholar]
  22. Nishi R., Berg D. K. Survival and development of ciliary ganglion neurones grown alone in cell culture. Nature. 1979 Jan 18;277(5693):232–234. doi: 10.1038/277232a0. [DOI] [PubMed] [Google Scholar]
  23. Paravicini U., Stoeckel K., Thoenen H. Biological importance of retrograde axonal transport of nerve growth factor in adrenergic neurons. Brain Res. 1975 Feb 7;84(2):279–291. doi: 10.1016/0006-8993(75)90982-8. [DOI] [PubMed] [Google Scholar]
  24. Reynolds C. P., Perez-Polo J. R. Induction of neurite outgrowth in the IMR-32 human neuroblastoma cell line by nerve growth factor. J Neurosci Res. 1981;6(3):319–325. doi: 10.1002/jnr.490060307. [DOI] [PubMed] [Google Scholar]
  25. Schubert D., LaCorbiere M., Whitlock C., Stallcup W. Alterations in the surface properties of cells responsive to nerve growth factor. Nature. 1978 Jun 29;273(5665):718–723. doi: 10.1038/273718a0. [DOI] [PubMed] [Google Scholar]
  26. 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]
  27. Stöckel K., Paravicini U., Thoenen H. Specificity of the retrograde axonal transport of nerve growth factor. Brain Res. 1974 Aug 23;76(3):413–421. doi: 10.1016/0006-8993(74)90818-x. [DOI] [PubMed] [Google Scholar]

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