Advertisement

Insulin-Like Growth Factors and Their Receptors in Muscle Development

  • Gyorgyi Szebenyi
  • Peter Rotwein
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 293)

Abstract

Insulin-like growth factors (IGF) I and II exert pleiotropic actions on target tissues. In muscle both IGF-I and II exhibit a range of physiological effects, including a concentration-dependent stimulation of metabolic functions such as glucose and amino acid uptake, acceleration of the rate of DNA synthesis, and enhancement of myoblast differentiation (1-4). The mitogenic and metabolic effects of the IGFs can be distinguished from their differentiation-promoting properties: the stimulation of differentiation persists in the presence of inhibitors of cell replication (5,6), and antisense myogenin oligonucleotides, which block IGF-l-induced differentiation, do not influence IGF-I stimulated metabolite uptake or proliferation (7). These observations imply that distinct signal-transduction pathways may be involved in each process.

Keywords

Lysosomal Enzyme Myoblast Differentiation Lysosomal Glycosidase Terminal Myogenic Differentiation Inositol Phosphate Turnover 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Beguinot, F., Kahn, C.R., Moses, A.C., and Smith, R.J. Distinct biologically active receptors for insulin, insulin-like growth factor I, and insulin-like growth factor II in cultured skeletal muscle cells. J. Biol. Chem. 260: 15892–15898, 1985.PubMedGoogle Scholar
  2. 2.
    Shimizu, M., Webster, C., Morgan, D.O., Blau, H.M., and Roth, R.A. Insulin and insulin-like growth factor receptors and responses in cultured human muscle cells. Am. J. Physiol. 251: E611–E615, 1986.PubMedGoogle Scholar
  3. 3.
    Schmid, C., Steiner, T.,Froesch, E.R. Preferential enhancement of myoblast differentiation by insulin-like growth factors (IGF I and IGF II) in primary cultures of chicken embryonic cells. FEBS Letters 161: 117–121, 1983.PubMedCrossRefGoogle Scholar
  4. 4.
    Ewton, D.Z., Falen, S.L, and Florini, J.R. The type II insulin-like growth factor (IGF) receptor has low affinity for IGF-I analogs: Pleiotypic actions of IGFs on myoblasts are apparently mediated by the type I receptor. Endocrinol. 120: 115–123, 1987.CrossRefGoogle Scholar
  5. 5.
    Turo, K.A., and Florini, J.R. Hormonal stimulation of myoblast differentiation in the absence of DNA synthesis. Am. J. Phyiol. 243: C278–284, 1982.Google Scholar
  6. 6.
    Florini, J.R., Ewton, D.Z., Falen, S.L., and Van Wyk, J.J. Biphasic concentration dependency of stimulation of myoblast differentiation by somatomedins. Am. J. Physiol. 250: C771–C778, 1986.PubMedGoogle Scholar
  7. 7.
    Florini, J.R., and Ewton, D.Z. Highly specific inhibition of IGF-l-stimulated differentiation by an antisense oligodeoxyribonucleo-tide to myogenin mRNA. J. Biol. Chem. 265: 13435–13437, 1990.PubMedGoogle Scholar
  8. 8.
    Clairmont, K.B., and Czech, M.P. Chicken and Xenopus mannose 6-phosphate receptors fail to bind insulin-like growth factor II. J. Biol. Chem. 264: 16390–16392, 1989.PubMedGoogle Scholar
  9. 9.
    Canfield, W.M., and Kornfeld, S. The chicken liver cation-independent mannose 6-phosphate receptor lacks the high affinity binding site for insulinlike growth factor II. J. Biol. Chem. 264: 7100–7103, 1989.PubMedGoogle Scholar
  10. 10.
    Kiess, W., Haskell, J.F., Lee, L, Greenstein, L.A., Miller, B.E., Aarons, A.L., Rechler, M.M., and Nissley, S.P. An antibody that blocks insulin-like growth factor (IGF) binding to the type II IGF receptor is neither an agonist nor an inhibitor of IGF-stimulated biologic responses in L6 myoblasts. J. Biol. Chem. 262: 12745–12754, 1987.PubMedGoogle Scholar
  11. 11.
    Czech, M.P. Signal transmission by the insulin-like growth factors. Cell 59: 235–238, 1989.PubMedCrossRefGoogle Scholar
  12. 12.
    Okamoto, T., Katada, T., Murayama, Y., Ui, M., Ogata, E., and Nishimoto, I. A simple structure encodes G protein-activating function of the IGF-ll/mannose 6-phosphate receptor. Cell 62: 709–717, 1990.PubMedCrossRefGoogle Scholar
  13. 13.
    Rogers, S.A., and Hammerman, M.R. Mannose 6-phosphate potentiates insulin-like growth factor ll-stimulated inositol triphosphate production by proximal tubular basolateral membranes. J. Biol. Chem. 264: 4273r4276, 1989.Google Scholar
  14. 14.
    Nishimoto, I., Hata, Y., Ogata, E., and Kojima, I. Insulin-like growth factor II stimulates calcium influx in competent BALB/c 3T3 cells primed with epidermal growth factor. J. Biol. Chem. 262: 12120–12126, 1987.PubMedGoogle Scholar
  15. 15.
    Kiess, W., Thomas, C.L., Greenstein, L.A., Lee, L, Sklar, M.M., Rechler, M.M., Sahagian, G.G., and Nissley, S.P. Insulin-like growth factor-ll (IGF-II) inhibits both the cellular uptake of β-galactosidase and the binding of β-galactosidase to purified IGF-ll/mannose 6-phosphate receptor. J. Biol. Chem. 264: 4710–4714, 1989.PubMedGoogle Scholar
  16. 16.
    Braulke, T., Tippmer, S., Chao, H-J., and von Figura, K. Insulin-like growth factors I and II stimulate endocytosis but do not affect sorting of lysosomal enzymes in human fibroblasts. J. Biol. Chem. 265: 6650–6655, 1990.PubMedGoogle Scholar
  17. 17.
    Dodson, M.V., Allen, R.E., and Hossner, K.L. Ovine somatomedin, multiplication-stimulating activity, and insulin promote skeletal muscle satellite cell proliferationin vitro. Endocrinol. 117: 2357–2363, 1985.CrossRefGoogle Scholar
  18. 18.
    Yaffe, D., and Saxel, O. Serial passaging and differentiation of myogenic cells isolated from dystrophic mouse muscle. Nature 270: 725–727, 1977.PubMedCrossRefGoogle Scholar
  19. 19.
    Tollefsen, S.E., Sadow, J.L, and Rotwein, P. Coordinate expression of insulinlike growth factor II and its receptor during muscle differentiation. Proc. Natl. Acad. Sci. USA 86: 1543–1547, 1989.PubMedCrossRefGoogle Scholar
  20. 20.
    Tollefsen, S.E., Lajara, R., McCusker, R.H., Clemmons, D.R., and Rotwein, P. Insulin-like growth factors (IGF) in muscle development. J. Biol. Chem. 264: 13810–13817, 1989.PubMedGoogle Scholar
  21. 21.
    Warren, L. Stimulated secretion of lysosomal enzymes by cells in culture. J. Biol. Chem. 264: 8835–8842, 1989.PubMedGoogle Scholar
  22. 22.
    Chirgwin, J.M., Przybyla, A.E., MacDonald, R.J., and Rutter, W.J. Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochem. 24: 5294–5299, 1979.Google Scholar
  23. 23.
    Rotwein, P., Burgess, S.K., Milbrandt, J.D., andd Krause, J.E. Differential expression of insulin-like growth factor genes in rat central nervous system. Proc. Natl. Acad. Sci. USA 85: 265–269, 1988.PubMedCrossRefGoogle Scholar
  24. 24.
    Szebenyi, G., and Rotwein, P. submitted.Google Scholar
  25. 25.
    Kornfeld, S. and Mellman, I. The biogenesis of lysosomes. Annu. Rev. Cell Biol. 5: 483–525, 1989.CrossRefGoogle Scholar
  26. 26.
    Newman, P.J., Gorski, J., White, G.C., Gidwitz, S., Cretney, C. J., and Aster, R.H. Enzymatic amplification of platelet-specific messenger RNA using the polymerase chain reaction. J. Clin. Invest. 82: 739–743, 1988.PubMedCrossRefGoogle Scholar
  27. 27.
    Pohlmann, R., Nagbi, G., Schmidt, B., Stein, M., Lorkowski, G., Krentler, C., Cully, J., Meyer, H.E., Grzeschik, K-H., Mersmann, G., Hasilik, A., and von Figura, K. Cloning of a cDNA encoding the human cation-dependent mannose 6-phosphate-specific receptor. Proc. Natl. Acad. Sci. USA 84:5575–5579, 1987.PubMedCrossRefGoogle Scholar
  28. 28.
    Dahms, N.M., Lobel, P., Breitmeyer, J., Chirgwin, J.M., and Kornfeld, S. 46 kd mannose 6-phosphate receptor: Cloning, expression, and homology to the 215 kd mannose 6-phosphate receptor. Cell 50: 181–192, 1987.PubMedCrossRefGoogle Scholar
  29. 29.
    Chan, S.J., Segundo, B.S., McCormick, M.B., and Steiner, D.F. Nucleotide and predicted amino acid sequences of cloned human and mouse preprocathepsin B cDNAs. Proc. Natl. Acad. Sci. USA. 83: 7721–7725, 1986.PubMedCrossRefGoogle Scholar
  30. 30.
    Joseph, L.J., Chang, L.C., Stamenkovich, D., and Sukhatme, V.P. Complete nucleotide and deduced amino acid sequences of human and murine preprocathepsin L. J. Clin. Invest. 81: 1621–1629, 1988.CrossRefGoogle Scholar
  31. 31.
    Bapat, B., Ethier, M., Neote, K., Mahuran, D., and Gravel, R.A. Cloning and sequence analysis of a CDNA encoding the β-subunit of mousep- hexosaminidase. FEBS Letters 237: 191–195, 1988.PubMedCrossRefGoogle Scholar
  32. 32.
    Baxter, R.C., and Martin, J.L. Binding proteins for the insulin-like growth factors: Structure, regulation and function. Progress in Growth Factor Research, 1: 49–68, 1989.PubMedCrossRefGoogle Scholar
  33. 33.
    Brewer, M.T., Stetler, G.L., Squires, C.H., Thompson, R.C., Busby, W.H., and Clemmons, D.R. Cloning, characterization, and expression of a human insulinlike growth factor binding protein. Biochem. Biophys. Res. Comm. 152: 1289–1297, 1988.PubMedCrossRefGoogle Scholar
  34. 34.
    Brown, A.L., Chiariotti, L, Orlowski, C.C., Mehlman, T., Burgess, W.H., Ackerman, E.J., Bruni, C.B., and Rechler, M.M. Nucleotide sequence and expression of a cDNA clone encoding a fetal rat binding protein for insulinlike growth factors. J. Biol. Chem. 264: 5148–5154, 1989.PubMedGoogle Scholar
  35. 35.
    De Vroede, M.A., Romanus, J.A., Standaert, M.L., Pollet, R.J., Nissley, S.P., and Rechler, M.M. Interaction of insulin-like growth factors with a nonfusing mouse muscle cell line: Binding, action, and receptor down-regulation. Endocrinol. 114: 1917–1929, 1984.CrossRefGoogle Scholar

Copyright information

© Plenum Press, New York 1991

Authors and Affiliations

  • Gyorgyi Szebenyi
    • 1
  • Peter Rotwein
    • 1
  1. 1.Departments of Medicine and Genetics Division of Biology and Biomedical ScienceWashington University School of MedicineSt. LouisUSA

Personalised recommendations