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Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1984 Apr;81(8):2562–2566. doi: 10.1073/pnas.81.8.2562

Insulin and insulin-like growth factor II permit nerve growth factor binding and the neurite formation response in cultured human neuroblastoma cells.

E Recio-Pinto, F F Lang, D N Ishii
PMCID: PMC345103  PMID: 6326132

Abstract

In serum-free medium, SH-SY5Y human neuroblastoma cells specifically and reversibly lost the capacity to bind 125I-labeled nerve growth factor (NGF) to the high-affinity sites (slow sites) and to respond by neurite outgrowth, unless physiological concentrations of insulin or insulin-like growth factor II were present. In serum-containing medium, anti-insulin antiserum decreased the neurite formation response to NGF, and insulin supplementation increased the number of available NGF slow sites. The low-affinity NGF fast sites are absent from SH-SY5Y cells and did not emerge on treatment with insulin. Insulin potentiated the induction of neurites by NGF in rat pheochromocytoma PC12 cells also. These results implicate a wider role for insulin and its homologs in the nervous system.

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Selected References

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  1. Acquaviva A. M., Bruni C. B., Nissley S. P., Rechler M. M. Cell-free synthesis of rat insulin-like growth factor II. Diabetes. 1982 Jul;31(7):656–658. doi: 10.2337/diab.31.7.656. [DOI] [PubMed] [Google Scholar]
  2. 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]
  3. Biedler J. L., Roffler-Tarlov S., Schachner M., Freedman L. S. Multiple neurotransmitter synthesis by human neuroblastoma cell lines and clones. Cancer Res. 1978 Nov;38(11 Pt 1):3751–3757. [PubMed] [Google Scholar]
  4. Bothwell M. Insulin and somatemedin MSA promote nerve growth factor-independent neurite formation by cultured chick dorsal root ganglionic sensory neurons. J Neurosci Res. 1982;8(2-3):225–231. doi: 10.1002/jnr.490080212. [DOI] [PubMed] [Google Scholar]
  5. Bottenstein J. E., Skaper S. D., Varon S. S., Sato G. H. Selective survival of neurons from chick embryo sensory ganglionic dissociates utilizing serum-free supplemented medium. Exp Cell Res. 1980 Jan;125(1):183–190. doi: 10.1016/0014-4827(80)90202-5. [DOI] [PubMed] [Google Scholar]
  6. Burstein D. E., Greene L. A. Evidence for RNA synthesis-dependent and -independent pathways in stimulation of neurite outgrowth by nerve growth factor. Proc Natl Acad Sci U S A. 1978 Dec;75(12):6059–6063. doi: 10.1073/pnas.75.12.6059. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Burton L. E., Wilson W. H., Shooter E. M. Nerve growth factor in mouse saliva. Rapid isolation procedures for and characterization of 7 S nerve growth factor. J Biol Chem. 1978 Nov 10;253(21):7807–7812. [PubMed] [Google Scholar]
  8. Claude P., Hawrot E., Dunis D. A., Campenot R. B. Binding, internalization, and retrograde transport of 125I-nerve growth factor in cultured rat sympathetic neurons. J Neurosci. 1982 Apr;2(4):431–442. doi: 10.1523/JNEUROSCI.02-04-00431.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Cohen P., Sutter A., Landreth G., Zimmermann A., Shooter E. M. Oxidation of tryptophan-21 alters the biological activity and receptor binding characteristics of mouse nerve growth factor. J Biol Chem. 1980 Apr 10;255(7):2949–2954. [PubMed] [Google Scholar]
  10. Cuatrecasas P., Hollenberg M. D., Chang K. J., Bennett V. Hormone receptor complexes and their modulation of membrane function. Recent Prog Horm Res. 1975;31:37–94. doi: 10.1016/b978-0-12-571131-9.50006-2. [DOI] [PubMed] [Google Scholar]
  11. Greene L. A. Nerve growth factor prevents the death and stimulates the neuronal differentiation of clonal PC12 pheochromocytoma cells in serum-free medium. J Cell Biol. 1978 Sep;78(3):747–755. doi: 10.1083/jcb.78.3.747. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. 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]
  13. Harper G. P., Thoenen H. Nerve growth factor: biological significance, measurement, and distribution. J Neurochem. 1980 Jan;34(1):5–16. doi: 10.1111/j.1471-4159.1980.tb04615.x. [DOI] [PubMed] [Google Scholar]
  14. 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]
  15. Ishii D. N. Effect of the suspected tumor promoters saccharin, cyclamate, and phenol on nerve growth factor binding and response in cultured embryonic chick ganglia. Cancer Res. 1982 Feb;42(2):429–432. [PubMed] [Google Scholar]
  16. Ishii D. N. Effect of tumor promoters on the response of cultured embryonic chick ganglia to nerve growth factor. Cancer Res. 1978 Nov;38(11 Pt 1):3886–3893. [PubMed] [Google Scholar]
  17. Ishii D. N. Inhibition of iodinated nerve growth factor binding by the suspected tumor promoters saccharin and cyclamate. J Natl Cancer Inst. 1982 Feb;68(2):299–303. [PubMed] [Google Scholar]
  18. Ishii D. N., Shooter E. M. Regulation of nerve growth factor synthesis in mouse submaxillary glands by testosterone. J Neurochem. 1975 Dec;25(6):843–851. doi: 10.1111/j.1471-4159.1975.tb04416.x. [DOI] [PubMed] [Google Scholar]
  19. Landreth G. E., Shooter E. M. Nerve growth factor receptors on PC12 cells: ligand-induced conversion from low- to high-affinity states. Proc Natl Acad Sci U S A. 1980 Aug;77(8):4751–4755. doi: 10.1073/pnas.77.8.4751. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Mobley W. C., Server A. C., Ishii D. N., Riopelle R. J., Shooter E. M. Nerve growth factor (first of three parts). N Engl J Med. 1977 Nov 17;297(20):1096–1104. doi: 10.1056/NEJM197711172972005. [DOI] [PubMed] [Google Scholar]
  21. Mobley W. C., Server A. C., Ishii D. N., Riopelle R. J., Shooter E. M. Nerve growth factor (third of three parts). N Engl J Med. 1977 Dec 1;297(22):1211–1218. doi: 10.1056/NEJM197712012972205. [DOI] [PubMed] [Google Scholar]
  22. Olender E. J., Stach R. W. Sequestration of 125I-labeled beta nerve growth factor by sympathetic neurons. J Biol Chem. 1980 Oct 10;255(19):9338–9343. [PubMed] [Google Scholar]
  23. Olender E. J., Wagner B. J., Stach R. W. Sequestration of 125I-labeled beta nerve growth factor by embryonic sensory neurons. J Neurochem. 1981 Aug;37(2):436–442. doi: 10.1111/j.1471-4159.1981.tb00474.x. [DOI] [PubMed] [Google Scholar]
  24. Perez-Polo J. R., Werbach-Perez K., Tiffany-Castiglioni E. A human clonal cell line model of differentiating neurons. Dev Biol. 1979 Aug;71(2):341–355. doi: 10.1016/0012-1606(79)90174-x. [DOI] [PubMed] [Google Scholar]
  25. Rinderknecht E., Humbel R. E. Primary structure of human insulin-like growth factor II. FEBS Lett. 1978 May 15;89(2):283–286. doi: 10.1016/0014-5793(78)80237-3. [DOI] [PubMed] [Google Scholar]
  26. Rinderknecht E., Humbel R. E. The amino acid sequence of human insulin-like growth factor I and its structural homology with proinsulin. J Biol Chem. 1978 Apr 25;253(8):2769–2776. [PubMed] [Google Scholar]
  27. STEPHENSON R. P. A modification of receptor theory. Br J Pharmacol Chemother. 1956 Dec;11(4):379–393. doi: 10.1111/j.1476-5381.1956.tb00006.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Schechter A. L., Bothwell M. A. Nerve growth factor receptors on PC12 cells: evidence for two receptor classes with differing cytoskeletal association. Cell. 1981 Jun;24(3):867–874. doi: 10.1016/0092-8674(81)90112-4. [DOI] [PubMed] [Google Scholar]
  29. Snyder E. Y., Kim S. U. Insulin: is it a nerve survival factor? Brain Res. 1980 Sep 8;196(2):565–571. doi: 10.1016/0006-8993(80)90426-6. [DOI] [PubMed] [Google Scholar]
  30. Sonnenfeld K. H., Ishii D. N. Nerve growth factor effects and receptors in cultured human neuroblastoma cell lines. J Neurosci Res. 1982;8(2-3):375–391. doi: 10.1002/jnr.490080226. [DOI] [PubMed] [Google Scholar]
  31. Spinelli W., Ishii D. N. Tumor promoter receptors regulating neurite formation in cultured human neuroblastoma cells. Cancer Res. 1983 Sep;43(9):4119–4125. [PubMed] [Google Scholar]
  32. Spinelli W., Sonnenfeld K. H., Ishii D. N. Effects of phorbol ester tumor promoters and nerve growth factor on neurite outgrowth in cultured human neuroblastoma cells. Cancer Res. 1982 Dec;42(12):5067–5073. [PubMed] [Google Scholar]
  33. Vinores S., Guroff G. Nerve growth factor: mechanism of action. Annu Rev Biophys Bioeng. 1980;9:223–257. doi: 10.1146/annurev.bb.09.060180.001255. [DOI] [PubMed] [Google Scholar]
  34. Zapf J., Schoenle E., Froesch E. R. Insulin-like growth factors I and II: some biological actions and receptor binding characteristics of two purified constituents of nonsuppressible insulin-like activity of human serum. Eur J Biochem. 1978 Jun 15;87(2):285–296. doi: 10.1111/j.1432-1033.1978.tb12377.x. [DOI] [PubMed] [Google Scholar]
  35. Zimmermann A., Sutter A., Shooter E. M. Monoclonal antibodies against beta nerve growth factor and their effects on receptor binding and biological activity. Proc Natl Acad Sci U S A. 1981 Jul;78(7):4611–4615. doi: 10.1073/pnas.78.7.4611. [DOI] [PMC free article] [PubMed] [Google Scholar]

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