Neurochemical Research

, Volume 17, Issue 10, pp 1041–1048 | Cite as

A factor derived from chick embryo retina which inhibits DNA synthesis of retina itself

  • Giuseppe Calvaruso
  • Renza Vento
  • Gennaro Taibi
  • Michela Giuliano
  • Giovanni Tesoriere
Original Articles

Abstract

Chick embryo retinas contain a peptide factor that inhibits DNA synthesis in explants of chick embryo retina. The inhibitory factor, obtained by acid/ethanol extraction from 15-day-old chick embryo retinas, was partially purified by affinity chromatography on heparin-sepharose CL-6B and gel filtration on Sephadex G-100. The inhibitor reduced DNA synthesis with maximal effects observed in retinal explants from 7 to 8-day-old chick embryos. The inhibitory effect became apparent after 10 h of incubation and reached the maximum levels after 16 h. DNA-inhibiting activity was heat and acid-stable and was destroyed by trypsin and alkaline treatments. The inhibitory effect was observed in retinal explants incubated in a medium free froml-glutamine, and the addition of this compound to the medium reduced the inhibitory effect in a concentration-dependent manner.

Key Words

Chick embryo retina development inhibitory factors retinal explants DNA synthesis 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Sporn, M.B., and Roberts, A.B. 1985. Autocrine growth factors and cancer. Nature 313:745–747.Google Scholar
  2. 2.
    Sporn, M.B., Roberts, A.B., Wakefield, L.M., and de Crombrugghe, B. 1987. Some recent advances in the chemistry and biology of transforming growth factor-beta. J. Cell Biol. 105:1039–1045.Google Scholar
  3. 3.
    Rizzino, A. 1988. Transforming growth factor-β: multiple effects on cell differentiation and extracellular matrices. Dev. Biol. 130:411–422.Google Scholar
  4. 4.
    Masui, T., Wakefield, L.M., Lechner, J.F., La Veck, M.A., Sporn, M.B., and Harris, C.C. 1986. Type beta transforming growth factor is the primary differentiation-inducing serum factor for normal human bronchial epithelial cells. Proc. Natl. Acad. Sci. USA. 83:2438–2442Google Scholar
  5. 5.
    Moses, H.L., Tucker, R.F., Leof, E.B., Coffey, R.J., Halper, J., and Shipley, G.D. 1985. Type beta transforming growth factor is a growth stimulator and a growth inhibitor. Cancer Cells (Cold Spring Harbor). 3:65–71.Google Scholar
  6. 6.
    Tucker, R.F., Shipley, G.D., Moses, H.L., and Holley, R.W. 1984. Growth inhibitor from BSC-1 cells closely related to platelet type beta transforming growth factor. Science 226:705–707.Google Scholar
  7. 7.
    Baird, A., and Durkin, T. 1986. Inhibition of endothelial cell proliferation by type-beta transforming growth factor: interactions with acidic and basic fibroblast growth factors. Biochem. Biophys. Res. Commun. 138:476–482.Google Scholar
  8. 8.
    Heimark, R.L., Twardzik, D.R., and Schwartz S.M. 1986. Inhibition of endothelial regeneration by type-beta transforming growth factor from platelets. Science 233:1078–1080.Google Scholar
  9. 9.
    Kehrl, J.H., Roberts, A.B., Wakefield, L.M., Jakowlew, S.B., Sporn, M.B., and Fauci, A.S. 1986. Transforming growth factor beta is an important immunomodulatory protein for human B-lymphocytes. J. Immunol. 137:3855–3860.Google Scholar
  10. 10.
    Kehrl, J.H., Wakefield, L.M., Roberts, A.B., Jakowlew, S.B., Alvarez-Mon, M., Derynck, R., Sporn, M.B., and Fauci, A.S. 1986. Production of transforming growth factor beta by human T lymphocytes and its potential role in the regulation of T cell growth. J. Exp. Med. 163:1037–1050.Google Scholar
  11. 11.
    Knabbe, C., Lippman, M.E., Wakefield, L.M., Flanders, K.C., Kasid, A., Derynck, R., and Dickson, R.B. 1987. Evidence that transforming growth factor-beta is a hormonally regulated negative growth factor in human breast cancer cells. Cell. 48:417–428.Google Scholar
  12. 12.
    Roberts, A.B., Anzano, M.A., Wakefield, L.M., Roche, N.S., Stern, D.F., and Sporn, M.B. 1985. Type β transforming growth factor: A bifunctional regulator of cellular growth. Proc. Natl. Acad. Sci. USA 82:119–123.Google Scholar
  13. 13.
    Mustoe, T.A., Pierce, G.F., Thomason, A., Gramates, P., Sporn, M.B., and Deuell, T.F. 1987. Accelerated healing of incisional wounds in rats induced by transforming growth factor-β. Science 237:1333–1335.Google Scholar
  14. 14.
    Globus, R.K., Patterson-Buckendahl, P., and Gospodarowicz, D. 1987. Regulation of bovine bone cell proliferation by fibroblast growth factor and transforming growth factor β. Endocrinology 123:98–105.Google Scholar
  15. 15.
    Chenu, C., Pfeilschifter, J., Mundy, G.R., and Roodman, G.D. 1988. Transforming growth factor β inhibits formation of osteoclast-like cells in long-term marrow cultures. Proc. Natl. Acad. Sci. USA 85:5683–5687.Google Scholar
  16. 16.
    Ignotz, R. and Massagué, J. 1986. Transforming growth factor-beta stimulates the expression of fibronectin and collagen and their incorporation into the extracellular matrix. J. Biol. Chem. 261:4337–4345.Google Scholar
  17. 17.
    Roberts, A.B., Sporn, M.B., Assoian, R.K., Smith, J.M., Roche, N.S., Wakefield, L.M., Heine, U.I., Liotta, L.A., Falanga, V., Kehrl, J.H., and Fauci, A.S. 1986. Transforming growth factor type-beta: rapid induction of fibrosis and angiogenesis in vivo and stimulation of collagen formation in vitro. Proc. Natl. Acad. Sci. USA. 83:4167–4171.Google Scholar
  18. 18.
    Assoian, R.K., Komoriya, A., Meyers, C.A., Miller, D.M., and Sporn, M.B. 1983. Transforming growth factor-beta in human platelets. J. Biol. Chem. 258:7155–7160.Google Scholar
  19. 19.
    Frolik, C.A., Dart, L.L., Meyers, C.A., Smith, D.M., and Sporn, M.B. 1983. Purification and initial characterization of a type beta transforming growth factor from human placenta. Proc. Natl. Acad. Sci. USA 80:3676–3680.Google Scholar
  20. 20.
    Hanks, S.K., Armour, R., Baldwin, J.H., Maldonado, F., Spiess, J. and Holley, R.W. 1988. Amino acid sequence of the BSC-1 cell growth inhibitor (polyergin) deduced from the nucleotide sequence of the cDNA. Proc. Natl. Acad. Sci. USA. 85:79–82.Google Scholar
  21. 21.
    Derynck, R., Lindquist, P.B., Lee, A., Wen, D., Tamm, J., Graycar, J.L., Rhee, L., Mason, A.J., Miller, D.A., Coffey, R.J., Moses, H.L., and Chen, E.Y. 1988. A new type of transforming growth factor-β, TGF-β3. EMBO J. 7:3737–3743.Google Scholar
  22. 22.
    Jakowlew, S.B., Dillard, P.J., Sporn, M.B., and Roberts, A.B. 1988. Complementary deoxyribonucleic acid cloning of an mRNA encoding transforming growth factor-beta 4 from chicken embryo chondrocytes. Mol. Endocrinol. 2:1186–1195.Google Scholar
  23. 23.
    Mc Mahon, J.B., Farrelly, J.G., and Iype, P.T. 1982. Purification and properties of a rat liver protein that specifically inhibits the proliferation of nonmalignant epithelial cells from rat liver. Proc. Natl. Acad. Sci. 79:456–460.Google Scholar
  24. 24.
    Husu, Y.M., and Wang, J.L. 1986. Growth control in cultured 3T3 fibroblasts. V. Purification of an Mr 13,000 polypeptide responsible for growth inhibitory activity. J. Cell. Biol. 102:362–369.Google Scholar
  25. 25.
    Sharifi, B.G., Johnson, T.C., Khurana, V.K., Bascom, C.C., Fleenor, T.J., and Chou, H.H. 1986. Purification and characterization of a bovine cerebral cortex surface sialoglycopeptide that inhibits cell proliferation and metabolism. J. Neurochem. 46:461–469.Google Scholar
  26. 26.
    Bohmer, F.D., Kraft, R., Otto, A., Wernstedt, C., Hellman, U., Kurtz, A., Muller, T., Rohde, K., Etzold, G., Lehmann, W., Langer, P., Heldin, C.H., and Grosse, R. 1987. Identification of a polypeptide growth inhibitor from bovine mammary gland. J. Biol. Chem. 262:15137–15143.Google Scholar
  27. 27.
    Shipley, G.D., Pittelkow, M.R., Wille, J.J., Scott, R.E., and Moses, H.L. 1986. Reversible inhibition of normal human prokeratinocyte proliferation by type β transforming growth factor-growth inhibitor in serum-free medium. Cancer Res. 46:2068–2071.Google Scholar
  28. 28.
    Barnard, J.A., Beauchamp, R.D., Coffey, R.J., and Moses, H.A. 1989. Regulation of intestinal epithelial cell growth by transforming growth factor type β. Proc. Natl. Acad. Sci. USA 86:1578–1582.Google Scholar
  29. 29.
    Robey, P.G., Young, M.F., Flanders, K.C., Roche, N.S., Kondaiah, P., Reddi, A.H., Termine, J.D., Sporn, M.B., and Roberts, A.B. 1987. Osteoblast synthesize and respond to TGF-beta in vitro. J. Cell Biol. 105:457–463.Google Scholar
  30. 30.
    Vento, R., D'Ancona, G., Giuliano, M., Taibi, G., and Tesoriere, G. 1987. Influence of hydrocortisone on chick embryo retina development. J. Neurochem. 48:1693–1698.Google Scholar
  31. 31.
    Tesoriere, G., Vento, R., Taibi, G., Calvaruso, G., and Schiavo, M.R. 1989. Biochemical aspects of chick embryo retina development: the effects of glucocorticoids. J. Neurochem. 52:1487–1494.Google Scholar
  32. 32.
    Tesoriere, G., Vento, R., Calvaruso, G., Schiavo, M.R., Giuliano, M., and Taibi, G. 1989. Inhibition of DNA synthesis in chick embryo retinas, in vitro, by a factor from fetal bovine serum. Dev. Brain Res. 47:19–25.Google Scholar
  33. 33.
    Roberts, A.B., Lamb, L.C., Newton, D.L., Sporn, M.B., De Larco, J.E., and Todaro, G.J. 1980. Transforming growth factors: isolation of polypeptides from virally and chemically transformed cells by acid/ethanol extraction. Proc. Natl. Acad. Sci. USA 77:3494–3498.Google Scholar
  34. 34.
    Lowry, O.H., Rosebrough, N.J., Farr, A.L., and Randall, R.J. 1951. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193:265–275.Google Scholar
  35. 35.
    Kalckar, H.M., Ullrey, D.B., Laursen, R.A. 1980. Effects of combined glutamine and serum deprivation on glucose control of hexose transport in mammalian fibroblast cultures. Proc. Natl. Acad. Sci. USA 77:5958–5961.Google Scholar
  36. 36.
    Tesoriere, G., Vento, R., Calvaruso, G., Taibi, G., Giuliano, M. 1992. Identification of insulin in chick embryo retina during development and its inhibitory effect on DNA synthesis. J. Neurochem. 58:1353–1359.Google Scholar
  37. 37.
    D'Amore, P.A., and Klagsbrun, M. 1984. Endothelial cell mitogens derived from retina and hypothalamus: biochemical and biological similarities. J. Cell Biol. 99:1545–1549.Google Scholar
  38. 38.
    Ferrara, N., and Henzel, W.J. 1989. Pituitary follicular cells secrete a novel heparin-binding growth factor specific for vascular endothelial cells. Biochem. Biophys. Res. Commun. 161:851–858.Google Scholar
  39. 39.
    Kimchi, A., Wang, X., Weinberg, R.A., Cheifetz, S., and Massagué, J. 1988. Absence of TGF-β receptors and growth inhibitory responses in retinoblastoma cells. Science 240:196–199.Google Scholar
  40. 40.
    Rappolee, D.A., Mark, D., Banda, M.J., Werb, Z. 1988. Wound macrophages express TGF-α and other growth factors in vivo: analysis by mRNA phenotyping. Science 241:708–712.Google Scholar
  41. 41.
    Moscona, A.A. 1972. Induction of glutamine synthetase in embryonic neural retina: a model for the regulation of specific gene expression in embryonic cells, in Biochemistry of Cell Differentiation. Vol. 24: FEBS Symposium (Monroy A. and Tsanev R. eds.) pp. 1–23. Academic Press. London.Google Scholar

Copyright information

© Plenum Publishing Corporation 1992

Authors and Affiliations

  • Giuseppe Calvaruso
    • 1
  • Renza Vento
    • 1
  • Gennaro Taibi
    • 1
  • Michela Giuliano
    • 1
  • Giovanni Tesoriere
    • 1
  1. 1.Institute of Biological ChemistryUniversity of PalermoPoliclinicoItaly

Personalised recommendations