Skip to main content
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
. 1980 Nov;77(11):6644–6648. doi: 10.1073/pnas.77.11.6644

Sequential addition of platelet factor and plasma to BALB/c 3T3 fibroblast cultures stimulates somatomedin-C binding early in cell cycle.

D R Clemmons, J J Van Wyk, W J Pledger
PMCID: PMC350343  PMID: 6161369

Abstract

Recent studies have shown that confluent cultured fibroblasts must be rendered competent by a factor contained in platelets before they can respond to plasma components and progress from G0 to S phase of the cell cycle. Somatomedin-C is one of the components of platelet-poor plasma necessary for cell cycle progression, but other factors present in somatomedin-C-deficient plasma are also required. Because both competence and progression factors contained in somatomedin-C-deficient serum modulate somatomedin-C action in fibroblasts, this study was undertaken to examine their possible influence on the binding of 125I-labeled somatomedin-C. Exposure of BALB/c 3T3 fibroblasts to high concentrations of platelet-derived growth factor alone prevented the time-dependent decrease in somatomedin-C binding which occurs in serum-free medium. Lower concentrations of the growth factor or 5% (vol/vol) platelet-poor plasma reduced but did not abolish this decrease. In contrast, sequential addition of platelet-derived growth factor followed by platelet-poor plasma resulted in a 75% increase in 125I-labeled somatomedin-C binding over basal levels during the first 2 hr. Binding increased by 125% when somatomedin-C-deficient platelet-poor plasma was substituted for normal platelet-poor plasma. The hormonal induction of somatomedin-C receptors appears to be a mechanism whereby peptide growth factors such as platelet-derived growth factor may condition the cell to respond optimally to somatomedin-C.

Full text

PDF
6644

Selected References

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

  1. Aharonov A., Pruss R. M., Herschman H. R. Epidermal growth factor. Relationship between receptor regulation and mitogenesis in 3T3 cells. J Biol Chem. 1978 Jun 10;253(11):3970–3977. [PubMed] [Google Scholar]
  2. Antoniades H. N., Scher C. D. Radioimmunoassay of a human serum growth factor for Balb/c-3T3 cells: derivation from platelets. Proc Natl Acad Sci U S A. 1977 May;74(5):1973–1977. doi: 10.1073/pnas.74.5.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Antoniades H. N., Scher C. D., Stiles C. D. Purification of human platelet-derived growth factor. Proc Natl Acad Sci U S A. 1979 Apr;76(4):1809–1813. doi: 10.1073/pnas.76.4.1809. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Baker J. B., Barsh G. S., Carney D. H., Cunningham D. D. Dexamethasone modulates binding and action of epidermal growth factor in serum-free cell culture. Proc Natl Acad Sci U S A. 1978 Apr;75(4):1882–1886. doi: 10.1073/pnas.75.4.1882. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Carney D. H., Cunningham D. D. Role of specific cell surface receptors in thrombin-stimulated cell division. Cell. 1978 Dec;15(4):1341–1349. doi: 10.1016/0092-8674(78)90059-4. [DOI] [PubMed] [Google Scholar]
  6. Carpenter G., Cohen S. 125I-labeled human epidermal growth factor. Binding, internalization, and degradation in human fibroblasts. J Cell Biol. 1976 Oct;71(1):159–171. doi: 10.1083/jcb.71.1.159. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. D'Ercole A. J., Underwood L. E., Groelke J., Plet A. Leprechaunism: studies of the relationship among hyperinsulinism, insulin resistance, and growth retardation. J Clin Endocrinol Metab. 1979 Mar;48(3):495–502. doi: 10.1210/jcem-48-3-495. [DOI] [PubMed] [Google Scholar]
  8. Das M., Fox C. F. Molecular mechanism of mitogen action: processing of receptor induced by epidermal growth factor. Proc Natl Acad Sci U S A. 1978 Jun;75(6):2644–2648. doi: 10.1073/pnas.75.6.2644. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Frantz C. N., Stiles C. D., Scher C. D. The tumor promoter 12-O-tetradecanoyl-phorbol-13-acetate enhances the proliferative response of Balb/c-3T3 cells to hormonal growth factors. J Cell Physiol. 1979 Sep;100(3):413–424. doi: 10.1002/jcp.1041000305. [DOI] [PubMed] [Google Scholar]
  10. Gavin J. R., 3rd, Roth J., Neville D. M., Jr, de Meyts P., Buell D. N. Insulin-dependent regulation of insulin receptor concentrations: a direct demonstration in cell culture. Proc Natl Acad Sci U S A. 1974 Jan;71(1):84–88. doi: 10.1073/pnas.71.1.84. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Guinivan P., Ladda R. L. Decrease in epidermal growth factor receptor levels and production of material enhancing epidermal growth factor binding accompany the temperature-dependent changes from normal to transformed phenotype. Proc Natl Acad Sci U S A. 1979 Jul;76(7):3377–3381. doi: 10.1073/pnas.76.7.3377. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Hayashi I., Sato G. H. Replacement of serum by hormones permits growth of cells in a defined medium. Nature. 1976 Jan 15;259(5539):132–134. doi: 10.1038/259132a0. [DOI] [PubMed] [Google Scholar]
  13. Hollenberg M. D., Cuatrecasas P. Insulin and epidermal growth factor. Human fibroblast receptors related to deoxyribonucleic acid synthesis and amino acid uptake. J Biol Chem. 1975 May 25;250(10):3845–3853. [PubMed] [Google Scholar]
  14. Megyesi K., Kahn C. R., Roth J., Froesch E. R., Humbel R. E., Zapf J., Neville D. M., Jr Insulin and non-suppressible insulin-like activity (NSILA-s): evidence for separate plasma membrane receptor sites. Biochem Biophys Res Commun. 1974 Mar 15;57(1):307–315. doi: 10.1016/s0006-291x(74)80391-8. [DOI] [PubMed] [Google Scholar]
  15. Moses A. C., Nissley S. P., Passamani J., White R. M. Further characterization of growth hormone-dependent somatomedin-binding proteins in rat serum and demonstration of somatomedin-binding proteins produced by rat liver cells in culture. Endocrinology. 1979 Feb;104(2):536–546. doi: 10.1210/endo-104-2-536. [DOI] [PubMed] [Google Scholar]
  16. Pledger W. J., Stiles C. D., Antoniades H. N., Scher C. D. An ordered sequence of events is required before BALB/c-3T3 cells become committed to DNA synthesis. Proc Natl Acad Sci U S A. 1978 Jun;75(6):2839–2843. doi: 10.1073/pnas.75.6.2839. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Pledger W. J., Stiles C. D., Antoniades H. N., Scher C. D. Induction of DNA synthesis in BALB/c 3T3 cells by serum components: reevaluation of the commitment process. Proc Natl Acad Sci U S A. 1977 Oct;74(10):4481–4485. doi: 10.1073/pnas.74.10.4481. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Rechler M. M., Fryklund L., Nissley S., Hall K., Podskalny J. M., Skottner A., Moses A. C. Purified human somatomedin A and rat multiplication stimulating activity. Mitogens for cultured fibroblasts that cross-react with the same growth peptide receptors. Eur J Biochem. 1978 Jan 2;82(1):5–12. doi: 10.1111/j.1432-1033.1978.tb11991.x. [DOI] [PubMed] [Google Scholar]
  19. Rechler M. M., Nissley S. P., Podskalny J. M., Moses A. C., Fryklund L. Identification of a receptor for somatomedin-like polypeptides in human fibroblasts. J Clin Endocrinol Metab. 1977 May;44(5):820–831. doi: 10.1210/jcem-44-5-820. [DOI] [PubMed] [Google Scholar]
  20. Rechler M. M., Podskalny J. M., Nissley S. P. Interaction of multiplication-stimulating activity with chick embryo fibroblasts demonstrates a growth receptor. Nature. 1976 Jan 15;259(5539):134–136. doi: 10.1038/259134a0. [DOI] [PubMed] [Google Scholar]
  21. Scher C. D., Pledger W. J., Martin P., Antoniades H., Stiles C. D. Transforming viruses directly reduce the cellular growth requirement for a platelet derived growth factor. J Cell Physiol. 1978 Dec;97(3 Pt 1):371–380. doi: 10.1002/jcp.1040970312. [DOI] [PubMed] [Google Scholar]
  22. Schlessinger J., Shechter Y., Willingham M. C., Pastan I. Direct visualization of binding, aggregation, and internalization of insulin and epidermal growth factor on living fibroblastic cells. Proc Natl Acad Sci U S A. 1978 Jun;75(6):2659–2663. doi: 10.1073/pnas.75.6.2659. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Stiles C. D., Isberg R. R., Pledger W. J., Antoniades H. N., Scher C. D. Control of the Balb/c-3T3 cell cycle by nutrients and serum factors: analysis using platelet-derived growth factor and platelet-poor plasma. J Cell Physiol. 1979 Jun;99(3):395–405. doi: 10.1002/jcp.1040990314. [DOI] [PubMed] [Google Scholar]
  24. Sutter A., Riopelle R. J., Harris-Warrick R. M., Shooter E. M. Nerve growth factor receptors. Characterization of two distinct classes of binding sites on chick embryo sensory ganglia cells. J Biol Chem. 1979 Jul 10;254(13):5972–5982. [PubMed] [Google Scholar]
  25. Svoboda M. E., Van Wyk J. J., Klapper D. G., Fellows R. E., Grissom F. E., Schlueter R. J. Purification of somatomedin-C from human plasma: chemical and biological properties, partial sequence analysis, and relationship to other somatomedins. Biochemistry. 1980 Feb 19;19(4):790–797. doi: 10.1021/bi00545a027. [DOI] [PubMed] [Google Scholar]
  26. Thomopoulos P., Roth J., Lovelace E., Pastan I. Insulin receptors in normal and transformed fibroblasts: relationship to growth and transformation. Cell. 1976 Jul;8(3):417–423. doi: 10.1016/0092-8674(76)90154-9. [DOI] [PubMed] [Google Scholar]
  27. Vogel A., Raines E., Kariya B., Rivest M. J., Ross R. Coordinate control of 3T3 cell proliferation by platelet-derived growth factor and plasma components. Proc Natl Acad Sci U S A. 1978 Jun;75(6):2810–2814. doi: 10.1073/pnas.75.6.2810. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Zapf J., Mäder M., Waldvogel M., Schalch D. S., Froesch E. R. Specific binding of nonsupressible insulinlike activity to chicken embryo fibroblasts and to a solubilized fibroblast receptor. Arch Biochem Biophys. 1975 Jun;168(2):630–637. doi: 10.1016/0003-9861(75)90295-7. [DOI] [PubMed] [Google Scholar]
  29. Zapf J., Rinderknecht E., Humbel R. E., Froesch E. R. Nonsuppressible insulin-like activity (NSILA) from human serum: recent accomplishments and their physiologic implications. Metabolism. 1978 Dec;27(12):1803–1828. doi: 10.1016/0026-0495(78)90267-6. [DOI] [PubMed] [Google Scholar]
  30. 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]

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