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
. 1986 Feb;83(3):822–826. doi: 10.1073/pnas.83.3.822

Insulin-like growth factor I/somatomedin C: a potent inducer of oligodendrocyte development.

F A McMorris, T M Smith, S DeSalvo, R W Furlanetto
PMCID: PMC322957  PMID: 3511475

Abstract

Cell cultures established from cerebrum of 1-day-old rats were used to investigate hormonal regulation of the development of oligodendrocytes, which synthesize myelin in the central nervous system. The number of oligodendrocytes that developed was preferentially increased by insulin, or by insulin-like growth factor I (IGF-I), also known as somatomedin C. High concentrations (5 micrograms/ml) of insulin were required for substantial induction of oligodendrocyte development, whereas only 3.3 ng of IGF-I per ml was needed for a 2-fold increase in oligodendrocyte numbers. At an IGF-I concentration of 100 ng/ml, oligodendrocyte numbers were increased 6-fold in cultures grown in the presence of 10% fetal bovine serum, or up to 60-fold in cultures maintained in serum-free medium. IGF-I produced less than a 2-fold increase in the number of nonoligodendroglial cells in the same cultures. Type I IGF receptors were identified on oligodendrocytes and on a putative oligodendrocyte precursor cell population identified by using mouse monoclonal antibody A2B5. These results indicate that IGF-I is a potent inducer of oligodendrocyte development and suggest a possible mechanism based on IGF deficiency for the hypomyelination that results from early postnatal malnutrition.

Full text

PDF
822

Images in this article

824Image
on p.824
824Image
on p.824
825Image
on p.825
825Image
on p.825
825Image
on p.825

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. Abney E. R., Williams B. P., Raff M. C. Tracing the development of oligodendrocytes from precursor cells using monoclonal antibodies, fluorescence-activated cell sorting, and cell culture. Dev Biol. 1983 Nov;100(1):166–171. doi: 10.1016/0012-1606(83)90207-5. [DOI] [PubMed] [Google Scholar]
  3. D'Ercole A. J., Stiles A. D., Underwood L. E. Tissue concentrations of somatomedin C: further evidence for multiple sites of synthesis and paracrine or autocrine mechanisms of action. Proc Natl Acad Sci U S A. 1984 Feb;81(3):935–939. doi: 10.1073/pnas.81.3.935. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Daughaday W. H. Hormonal regulation of growth by somatomedin and other tissue growth factors. Clin Endocrinol Metab. 1977 Mar;6(1):117–135. doi: 10.1016/s0300-595x(77)80059-5. [DOI] [PubMed] [Google Scholar]
  5. Eccleston P. A., Silberberg D. H. The differentiation of oligodendrocytes in a serum-free hormone-supplemented medium. Brain Res. 1984 Sep;318(1):1–9. doi: 10.1016/0165-3806(84)90056-7. [DOI] [PubMed] [Google Scholar]
  6. Eisenbarth G. S., Walsh F. S., Nirenberg M. Monoclonal antibody to a plasma membrane antigen of neurons. Proc Natl Acad Sci U S A. 1979 Oct;76(10):4913–4917. doi: 10.1073/pnas.76.10.4913. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Eldred W. D., Zucker C., Karten H. J., Yazulla S. Comparison of fixation and penetration enhancement techniques for use in ultrastructural immunocytochemistry. J Histochem Cytochem. 1983 Feb;31(2):285–292. doi: 10.1177/31.2.6339606. [DOI] [PubMed] [Google Scholar]
  8. Froesch E. R., Schmid C., Schwander J., Zapf J. Actions of insulin-like growth factors. Annu Rev Physiol. 1985;47:443–467. doi: 10.1146/annurev.ph.47.030185.002303. [DOI] [PubMed] [Google Scholar]
  9. Furlanetto R. W., DiCarlo J. N. Somatomedin-C receptors and growth effects in human breast cells maintained in long-term tissue culture. Cancer Res. 1984 May;44(5):2122–2128. [PubMed] [Google Scholar]
  10. Furlanetto R. W. Pitfalls in the somatomedin-C radioimmunoassay. J Clin Endocrinol Metab. 1982 May;54(5):1084–1086. doi: 10.1210/jcem-54-5-1084. [DOI] [PubMed] [Google Scholar]
  11. Hsu S. M., Raine L., Fanger H. Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques: a comparison between ABC and unlabeled antibody (PAP) procedures. J Histochem Cytochem. 1981 Apr;29(4):577–580. doi: 10.1177/29.4.6166661. [DOI] [PubMed] [Google Scholar]
  12. Kasuga M., Van Obberghen E., Nissley S. P., Rechler M. M. Demonstration of two subtypes of insulin-like growth factor receptors by affinity cross-linking. J Biol Chem. 1981 Jun 10;256(11):5305–5308. [PubMed] [Google Scholar]
  13. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  14. 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]
  15. Massagué J., Czech M. P. The subunit structures of two distinct receptors for insulin-like growth factors I and II and their relationship to the insulin receptor. J Biol Chem. 1982 May 10;257(9):5038–5045. [PubMed] [Google Scholar]
  16. McCarthy K. D., de Vellis J. Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral tissue. J Cell Biol. 1980 Jun;85(3):890–902. doi: 10.1083/jcb.85.3.890. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. McMorris F. A. Cyclic AMP induction of the myelin enzyme 2',3'-cyclic nucleotide 3'-phosphohydrolase in rat oligodendrocytes. J Neurochem. 1983 Aug;41(2):506–515. doi: 10.1111/j.1471-4159.1983.tb04768.x. [DOI] [PubMed] [Google Scholar]
  18. McMorris F. A., Miller S. L., Pleasure D., Abramsky O. Expression of biochemical properties of oligodendrocytes in oligodendrocyte x glioma cell hybrids proliferating in vitro. Exp Cell Res. 1981 Jun;133(2):395–404. doi: 10.1016/0014-4827(81)90332-3. [DOI] [PubMed] [Google Scholar]
  19. Miekka S. I., Ingham K. C., Menache D. Rapid methods for isolation of human plasma fibronectin. Thromb Res. 1982 Jul 1;27(1):1–14. doi: 10.1016/0049-3848(82)90272-9. [DOI] [PubMed] [Google Scholar]
  20. Noguchi T., Sugisaki T., Takamatsu K., Tsukada Y. Factors contributing to the poor myelination in the brain of the Snell dwarf mouse. J Neurochem. 1982 Dec;39(6):1693–1699. doi: 10.1111/j.1471-4159.1982.tb08004.x. [DOI] [PubMed] [Google Scholar]
  21. Noguchi T., Sugisaki T., Tsukada Y. Postnatal action of growth and thyroid hormones on the retarded cerebral myelinogenesis of Snell dwarf mice (dw). J Neurochem. 1982 Jan;38(1):257–263. doi: 10.1111/j.1471-4159.1982.tb10878.x. [DOI] [PubMed] [Google Scholar]
  22. Pelton E. W., Grindeland R. E., Young E., Bass N. H. Effects of immunologically induced growth hormone deficiency on myelinogenesis in developing rat cerebrum. Neurology. 1977 Mar;27(3):282–288. doi: 10.1212/wnl.27.3.282. [DOI] [PubMed] [Google Scholar]
  23. Phillips L. S., Vassilopoulou-Sellin R. Nutritional regulation of somatomedin. Am J Clin Nutr. 1979 May;32(5):1082–1096. doi: 10.1093/ajcn/32.5.1082. [DOI] [PubMed] [Google Scholar]
  24. Phillips L. S., Vassilopoulou-Sellin R. Somatomedins (first of two parts). N Engl J Med. 1980 Feb 14;302(7):371–380. doi: 10.1056/NEJM198002143020704. [DOI] [PubMed] [Google Scholar]
  25. Phillips L. S., Vassilopoulou-Sellin R. Somatomedins (second of two parts). N Engl J Med. 1980 Feb 21;302(8):438–446. doi: 10.1056/NEJM198002213020805. [DOI] [PubMed] [Google Scholar]
  26. Phillips L. S., Young H. S. Nutrition and somatomedin. I. Effect of fasting and refeeding on serum somatomedin activity and cartilage growth activity in rats. Endocrinology. 1976 Jul;99(1):304–314. doi: 10.1210/endo-99-1-304. [DOI] [PubMed] [Google Scholar]
  27. Raff M. C., Miller R. H., Noble M. A glial progenitor cell that develops in vitro into an astrocyte or an oligodendrocyte depending on culture medium. Nature. 1983 Jun 2;303(5916):390–396. doi: 10.1038/303390a0. [DOI] [PubMed] [Google Scholar]
  28. Raff M. C., Mirsky R., Fields K. L., Lisak R. P., Dorfman S. H., Silberberg D. H., Gregson N. A., Leibowitz S., Kennedy M. C. Galactocerebroside is a specific cell-surface antigenic marker for oligodendrocytes in culture. Nature. 1978 Aug 24;274(5673):813–816. [PubMed] [Google Scholar]
  29. Ranscht B., Clapshaw P. A., Price J., Noble M., Seifert W. Development of oligodendrocytes and Schwann cells studied with a monoclonal antibody against galactocerebroside. Proc Natl Acad Sci U S A. 1982 Apr;79(8):2709–2713. doi: 10.1073/pnas.79.8.2709. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Rechler M. M., Nissley S. P. The nature and regulation of the receptors for insulin-like growth factors. Annu Rev Physiol. 1985;47:425–442. doi: 10.1146/annurev.ph.47.030185.002233. [DOI] [PubMed] [Google Scholar]
  31. Saida T., Saida K., Dorfman S. H., Silberberg D. H., Sumner A. J., Manning M. C., Lisak R. P., Brown M. J. Experimental allergic neuritis induced by sensitization with galactocerebroside. Science. 1979 Jun 8;204(4397):1103–1106. doi: 10.1126/science.451555. [DOI] [PubMed] [Google Scholar]
  32. Sara V. R., Hall K., Lins P. E., Fryklund L. Serum levels of immunoreactive somatomedin A in the rat: some developmental aspects. Endocrinology. 1980 Aug;107(2):622–625. doi: 10.1210/endo-107-2-622. [DOI] [PubMed] [Google Scholar]
  33. Sikes R. W., Fuller G. N., Colbert C., Chronister R. B., DeFrance J., Wiggins R. C. The relative numbers of oligodendroglia in different brain regions of normal and postnatally undernourished rats. Brain Res Bull. 1981 May;6(5):385–391. doi: 10.1016/s0361-9230(81)80008-1. [DOI] [PubMed] [Google Scholar]
  34. Sprinkle T. J., Grimes M. J., Eller A. G. Isolation of 2',3'-cyclic nucleotide 3'-phosphodiesterase from human brain. J Neurochem. 1980 Apr;34(4):880–887. doi: 10.1111/j.1471-4159.1980.tb09661.x. [DOI] [PubMed] [Google Scholar]
  35. Stuart C. A., Pietrzyk R., Siu A. K., Furlanetto R. W. Size discrepancy between somatomedin-C and insulin receptors. J Clin Endocrinol Metab. 1984 Jan;58(1):1–5. doi: 10.1210/jcem-58-1-1. [DOI] [PubMed] [Google Scholar]
  36. Wiggins R. C. Myelin development and nutritional insufficiency. Brain Res. 1982 Jun;257(2):151–175. doi: 10.1016/0165-0173(82)90016-9. [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