Skip to main content
NCBI home page
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
. 1991 Mar 15;88(6):2199–2203. doi: 10.1073/pnas.88.6.2199

Fibroblast growth factor-mediated proliferation of central nervous system precursors depends on endogenous production of insulin-like growth factor I.

J Drago 1, M Murphy 1, S M Carroll 1, R P Harvey 1, P F Bartlett 1
PMCID: PMC51197  PMID: 2006157

Abstract

Fibroblast growth factor stimulates proliferation and subsequent differentiation of precursor cells isolated from the neuroepithelium of embryonic day 10 mice in vitro. Here we show that fibroblast growth factor-induced proliferation is dependent on the presence of insulin-like growth factors (IGFs) and that IGF-I is endogenously produced by the neuroepithelial cells. Blocking of endogenous IGF-I activity with anti-IGF-I antibodies results in complete inhibition of fibroblast growth factor-mediated proliferation and in cell death. IGF-I alone acts as a survival agent. These observations correlate with the detection of transcripts for IGF-I and basic fibroblast growth factor in freshly isolated neuroepithelium and are consistent with an autocrine action of these factors in early brain development in vivo.

Full text

PDF
2199

Images in this article

2201Image
on p.2201
2202Image
on p.2202
2202Image
on p.2202
2202Image
on p.2202

Selected References

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

  1. Abney E. R., Bartlett P. P., Raff M. C. Astrocytes, ependymal cells, and oligodendrocytes develop on schedule in dissociated cell cultures of embryonic rat brain. Dev Biol. 1981 Apr 30;83(2):301–310. doi: 10.1016/0012-1606(81)90476-0. [DOI] [PubMed] [Google Scholar]
  2. Allen R. E., Boxhorn L. K. Regulation of skeletal muscle satellite cell proliferation and differentiation by transforming growth factor-beta, insulin-like growth factor I, and fibroblast growth factor. J Cell Physiol. 1989 Feb;138(2):311–315. doi: 10.1002/jcp.1041380213. [DOI] [PubMed] [Google Scholar]
  3. Bartlett P. F., Reid H. H., Bailey K. A., Bernard O. Immortalization of mouse neural precursor cells by the c-myc oncogene. Proc Natl Acad Sci U S A. 1988 May;85(9):3255–3259. doi: 10.1073/pnas.85.9.3255. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bassas L., de Pablo F., Lesniak M. A., Roth J. Ontogeny of receptors for insulin-like peptides in chick embryo tissues: early dominance of insulin-like growth factor over insulin receptors in brain. Endocrinology. 1985 Dec;117(6):2321–2329. doi: 10.1210/endo-117-6-2321. [DOI] [PubMed] [Google Scholar]
  5. Bell G. I., Stempien M. M., Fong N. M., Rall L. B. Sequences of liver cDNAs encoding two different mouse insulin-like growth factor I precursors. Nucleic Acids Res. 1986 Oct 24;14(20):7873–7882. doi: 10.1093/nar/14.20.7873. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Carlsson-Skwirut C., Lake M., Hartmanis M., Hall K., Sara V. R. A comparison of the biological activity of the recombinant intact and truncated insulin-like growth factor 1 (IGF-1). Biochim Biophys Acta. 1989 May 10;1011(2-3):192–197. doi: 10.1016/0167-4889(89)90209-7. [DOI] [PubMed] [Google Scholar]
  7. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987 Apr;162(1):156–159. doi: 10.1006/abio.1987.9999. [DOI] [PubMed] [Google Scholar]
  8. Czech M. P. Structural and functional homologies in the receptors for insulin and the insulin-like growth factors. Cell. 1982 Nov;31(1):8–10. doi: 10.1016/0092-8674(82)90399-3. [DOI] [PubMed] [Google Scholar]
  9. Drago J., Nurcombe V., Bartlett P. F. Laminin through its long arm E8 fragment promotes the proliferation and differentiation of murine neuroepithelial cells in vitro. Exp Cell Res. 1991 Jan;192(1):256–265. doi: 10.1016/0014-4827(91)90184-v. [DOI] [PubMed] [Google Scholar]
  10. Enberg G., Tham A., Sara V. R. The influence of purified somatomedins and insulin on foetal rat brain DNA synthesis in vitro. Acta Physiol Scand. 1985 Oct;125(2):305–308. doi: 10.1111/j.1748-1716.1985.tb07720.x. [DOI] [PubMed] [Google Scholar]
  11. Gurdon J. B. A community effect in animal development. Nature. 1988 Dec 22;336(6201):772–774. doi: 10.1038/336772a0. [DOI] [PubMed] [Google Scholar]
  12. Krieg P. A., Melton D. A. In vitro RNA synthesis with SP6 RNA polymerase. Methods Enzymol. 1987;155:397–415. doi: 10.1016/0076-6879(87)55027-3. [DOI] [PubMed] [Google Scholar]
  13. Lenoir D., Honegger P. Insulin-like growth factor I (IGF I) stimulates DNA synthesis in fetal rat brain cell cultures. Brain Res. 1983 Apr;283(2-3):205–213. doi: 10.1016/0165-3806(83)90177-3. [DOI] [PubMed] [Google Scholar]
  14. Moore R., Casey G., Brookes S., Dixon M., Peters G., Dickson C. Sequence, topography and protein coding potential of mouse int-2: a putative oncogene activated by mouse mammary tumour virus. EMBO J. 1986 May;5(5):919–924. doi: 10.1002/j.1460-2075.1986.tb04304.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Murphy M., Drago J., Bartlett P. F. Fibroblast growth factor stimulates the proliferation and differentiation of neural precursor cells in vitro. J Neurosci Res. 1990 Apr;25(4):463–475. doi: 10.1002/jnr.490250404. [DOI] [PubMed] [Google Scholar]
  16. Pfeifle B., Boeder H., Ditschuneit H. Interaction of receptors for insulin-like growth factor I, platelet-derived growth factor, and fibroblast growth factor in rat aortic cells. Endocrinology. 1987 Jun;120(6):2251–2258. doi: 10.1210/endo-120-6-2251. [DOI] [PubMed] [Google Scholar]
  17. Raff M. C. Glial cell diversification in the rat optic nerve. Science. 1989 Mar 17;243(4897):1450–1455. doi: 10.1126/science.2648568. [DOI] [PubMed] [Google Scholar]
  18. Reid H. H., Wilks A. F., Bernard O. Two forms of the basic fibroblast growth factor receptor-like mRNA are expressed in the developing mouse brain. Proc Natl Acad Sci U S A. 1990 Feb;87(4):1596–1600. doi: 10.1073/pnas.87.4.1596. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Risau W. Developing brain produces an angiogenesis factor. Proc Natl Acad Sci U S A. 1986 Jun;83(11):3855–3859. doi: 10.1073/pnas.83.11.3855. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Rotwein P., Burgess S. K., Milbrandt J. D., Krause J. E. Differential expression of insulin-like growth factor genes in rat central nervous system. Proc Natl Acad Sci U S A. 1988 Jan;85(1):265–269. doi: 10.1073/pnas.85.1.265. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Rotwein P., Pollock K. M., Didier D. K., Krivi G. G. Organization and sequence of the human insulin-like growth factor I gene. Alternative RNA processing produces two insulin-like growth factor I precursor peptides. J Biol Chem. 1986 Apr 15;261(11):4828–4832. [PubMed] [Google Scholar]
  22. Ruoslahti E. Proteoglycans in cell regulation. J Biol Chem. 1989 Aug 15;264(23):13369–13372. [PubMed] [Google Scholar]
  23. Russell W. E., Van Wyk J. J., Pledger W. J. Inhibition of the mitogenic effects of plasma by a monoclonal antibody to somatomedin C. Proc Natl Acad Sci U S A. 1984 Apr;81(8):2389–2392. doi: 10.1073/pnas.81.8.2389. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Saleh M., Bartlett P. F. Evidence from neuronal heterokaryons for a trans-acting factor suppressing Thy-1 expression during neuronal development. J Neurosci Res. 1989 Aug;23(4):406–415. doi: 10.1002/jnr.490230406. [DOI] [PubMed] [Google Scholar]
  25. Sara V. R., Carlsson-Skwirut C., Andersson C., Hall E., Sjögren B., Holmgren A., Jörnvall H. Characterization of somatomedins from human fetal brain: identification of a variant form of insulin-like growth factor I. Proc Natl Acad Sci U S A. 1986 Jul;83(13):4904–4907. doi: 10.1073/pnas.83.13.4904. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Sara V. R., King T. L., Stuart M. C., Lazarus L. Hormonal regulation of fetal brain cell proliferation: presence in serum of a trophin responsive to pituitary growth hormone stimulation. Endocrinology. 1976 Dec;99(6):1512–1518. doi: 10.1210/endo-99-6-1512. [DOI] [PubMed] [Google Scholar]
  27. Underwood L. E., D'Ercole A. J., Clemmons D. R., Van Wyk J. J. Paracrine functions of somatomedins. Clin Endocrinol Metab. 1986 Feb;15(1):59–77. doi: 10.1016/s0300-595x(86)80042-1. [DOI] [PubMed] [Google Scholar]
  28. Wilkinson D. G., Peters G., Dickson C., McMahon A. P. Expression of the FGF-related proto-oncogene int-2 during gastrulation and neurulation in the mouse. EMBO J. 1988 Mar;7(3):691–695. doi: 10.1002/j.1460-2075.1988.tb02864.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Wu D. K., Maciag T., de Vellis J. Regulation of neuroblast proliferation by hormones and growth factors in chemically defined medium. J Cell Physiol. 1988 Aug;136(2):367–372. doi: 10.1002/jcp.1041360222. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES