Abstract
IGF-I has long been known to have mitogenic effects on isolated skeletal tissue (Salmon and Daughaday, 1957) and insulin-like metabolic effects on isolated adipose tissue and muscle tissue (Froesch et al., 1966; Poggi et al., 1979). Stimulation of glucose utilization by IGF-I has been observed in vivo in rats and humans (Zapf et al., 1986; Guler et al., 1987). Moreover, Giacca et al. (1990) have demonstrated that skeletal muscle is the preferred site for the stimulation of glucose utilization by IGF-I in completely insulin-deficient diabetic dogs. Simultaneously, Moxely III et al. (1990) demonstrated that in vivo, IGF-I stimulates hexose uptake directly into rat muscles. These specific effects of IGF-I on skeletal muscle are consistent with the observation that skeletal muscle expresses abundant amounts of IGF-I receptors (Livingston et al., 1988, Dohm et al., 1990), whereas adipose tissue has very low numbers of IGF-I receptors (Rechler and Nissley, 1985; Sinha et al., 1990). Skeletal muscle is also the primary site of action for the stimulation of glucose utilization by insulin in vivo (Defronzo et al., 1981). Although IGF-I and insulin have common biological actions, IGF-I and insulin receptors may function independently. For example, rat 1 fibroblasts expressing a mutant insulin receptor with an inactive tyrosine kinase are unresponsive to insulin stimulation of glucose uptake but can still respond to IGF-I through their endogenous IGF-I receptors (McClain et al., 1990). Secondly, Lammers et al. (1989) demonstrated that chimeric receptors consisting of the extracellular insulin receptor domain and the intracellular IGF-I receptor domain were ten times more responsive to insulin for stimulation of DNA synthesis than was the native insulin receptor. This suggested that the intracellular kinase of the IGF-I receptor is more active than the insulin receptor kinase and is thus inherently different from its insulin receptor counterpart. Hence, IGF-I and insulin and their receptors share common responses but can trigger them independently.
This is a preview of subscription content, log in via an institution to check access.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Preview
Unable to display preview. Download preview PDF.
References
Baldwin, S.A., Baldwin, J.M., and Lienhard, G.E., 1982, Monosaccharide transporter of the human erythrocyte. Characterization of an improved preparation, Biochemistry, 21: 3836–3842.
Beguinot, F., Kahn, C.R., Moses, A.C., and Smith, R.J., 1985, Distinct biologically active receptors for insulin, insulin-like growth factor I and insulin-like gorwth factor II in cultured skeletal muscle cells, J. Biol. Chem., 260: 15892–15898.
Beguinot, F., Kahn, C.R., Moses, A.C., and Smith R.J., 198 6, The development of insulin receptors and responsiveness is an early marker of differentiation in the muscle cell line L6, Endocrinology, 118: 446–455.
Bilan, P.J., and Klip, A., 1990, Glycation of the human erythrocyte glucose transporterin vtiro and its functional consequences, Bjochem. J., 268: 661–667.
Birnbaum, M.J., 1989, Identification of a novel gene encoding an insulin-responsive glucose transporter protein, Cell, 57: 305–315.
Bradford, M.M., 1976, A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding, Anal. Biochem.,72: 248–254.
Burant, C.F., Treutelar, M.K., Allen, K.D., Sens, D.A., and Buse, M.G., 1987, Comparison of insulin and insulin-like growth factor I receptors from rat skeletal muscle and L6 myocytes, Biochem. Biophys. Res. Commnn.,147: 100–107.
Calderhead, D.M., Kitagawa, K., Lienhard, G.E., and Gould G.W., 1990, Translocation of the brain-type glucose transporter largely accounts for insulin stimulation of glucose transport in BC3H-1 myocytes, Biochem. J., 269: 597–601.
Defronzo, R.A., Ferranninni, E., Sato, Y., Felig, P., and Wahren, J., 1981, Synergistic interaction between exercise and insulin on peripheral glucose uptake, J. Clin. Invest., 68: 1468–1474.
Dohm, C.L., Elton, C.W., Raju, M.S., Mooney, N.D., Dimarchi, R., Pories, W.J., Flickinger, E.G., Atkinson, S.M. Jr., and Caro, J.F., 1990, IGF-I-Stimulated glucose transport in human skeletal muscle and IGF-I resistance in obesity and NIDDM, Diabetes, 39: 1028–1032.
Douen, A.G., Ramlal, T., Rastogi, S., Bilan, P.J., Cartee, G.D., Vranic, M., Holloszy, J.O., and Klip, A., 1990, Exercise induces recruitment of the insulin-responsive glucose transporter, J. Biol. Chem., 265:13427.
Froech, E.R., Muller, W.A., Burgi, H., Waldvogel, M., and Labhart, A., 1966, Nonsuppressable insulin-like activity of human serum. I. Physicochemical properties, extraction and partial purification, Biochim. Biophys. Acta, 121: 360–374.
Fushiki, T., Wells, J.A., Tapscott, E.B., and Dohm, G.L., 1989, Changes in glucose transporters in muscle in reponse to exercise, Am.J. Physiol., 256: E580-E587.
Giacca, A., Gupta, R., Efendic, S., Hall, K., Skottner, A., Lickley, L., and Vranic, M., 1990, Differential effects of IGF-I and insulin of glucoregulation and fat metabolism in depancreatized dogs, Diabetes, 39: 340–347.
Guler, H.P., Zapf, J., and Froesch, E.R., 1987, Short-term metabolic effects of recombinant human insulin-like growth factor I in healthy adults, N. Engl. J. Med., 317: 137–140.
Holman, G.D., and Rees, W.D., 1987, Photolabelling of the hexose transporter at external and internal sites: Fragmentation patterns and evidence for a conformational change, Biochim. Biophys. Acta, 897: 395–405.
James, D.E., Brown, R. Navarro, J., and Pilch, P.F., 1988, Insulin-regulatable tissues express a unique insulin-sensitive glucose transport protein, Nature, 333: 183–185.
James, D.E., Strube, M., and Mueckler, M., 1989, Molecular cloning and characterization of an insulin-regulatable glucose transporter, Nature, 338: 83–87.
Kidokoro, Y., 1975, Developmental Changes of membrane electrical properties in a rat skeletal muscle cell line, J. Physiol.(London)r 244: 129– 143.
Klip, A., Li, G., and Walker, D., 1983, Insulin binding to differentiating muscle cells in culture, Can. J. Biochem. Cell Biol., 61: 644–649.
Klip, A., Li, G., and Logan, W.J., 1984, Induction of sugar uptake response to insulin by serum depetion in fusing L6 myoblasts, Am. J. Physiol., 247: E291–E296.
Koivisto, U.-M., Martinez-Valdez, H., Bilan, P.J., Burdett, E., Ramlal, T., and Klip, A., Differential regulation of GLUT-1 and GLUT-4 transport systems by glucose and insulin in L6 muscle cells in culture, J. Biol. Chem. (in press) .
Laemmli, U.K., 1970, Cleavage of structural proteins during the assembly of the head of bacteriophage T4, Nature, 227, 680–685.
Lammers, R., Gray, A., Schlessinger, J., and Ullrich, A., 1989, Differential signalling potential of insulin and IGF-I receptor cytoplasmic domains, EMBO J.8: 1369–1375.
Livingston, N., Pollare, T., Lithell, H., and Arner, P., 1988, Characterization of insulin-like growth factor I receptor in skeletal muscles of normal and insulin resistant subjects, Diabetolocria. 31: 871–877.
Lowry, O.H., Rosebrough, N.J., Farr, A.L., Randall, R.J., 1951, Protein measurement with the folin phenol reagent, J. Biol. Chem., 193: 265– 275.
McClain, D.A., Maegawa, H., Thies, R.S., and Olefsky, J.M., 1990, Dissection of the growth versus metabolic effects of insulin and insulin-like growth factor-I in transfected cells expressing kinase-defective human insulin receptors, J. Biol. Chem., 265: 1678–1682.
Moxley III, R.T., Arner, P., Moss, A., Skottner, A., Fox, M., James, D., Livingston, J.N., 1990, Acute effects of insulin-like growth factor I and insulin on glucose metabolism in vivo, Am. J. Physiol., 259: E561–E567.
Poggi, C., Le Marchand-Brustel, Y., Zapf, J., Froesch, E.R., and Freychet, P., 1979, Effects and binding on insulin-like growth factor I (IGF I) in the isolated soleus muscle of lean and obese mice: Comparison with insulin, Endocrinology, 105: 723–730.
Ramlal, T., Sarabia, V., Bilan, P.J., and Klip, A., 1988, Insulin-mediated translocation of glucose transporters from intracellular membranes to plasma membranes: Sole mechanism of stimulation of glucose transport in L6 muscle cells, Biochem. Biophys. Res. Commun., 157: 1329–1335.
Rechler, M.M., and Nissley, S.P., 1985, The nature and regulation of the receptors for insulin-like growth factors, Ann. Rev. Physiol., 47: 425–442.
Ross, M., Francis, G.L., Szabo, L., Wallace, J.C., and Ballard, F.J., 1989, Insulin-like growth factor (IGF)-binding proteins inhibit the biological activities of IGF-1 and IGF-2 but not des-(1-3)-IGF-1, Biochem. J., 258: 267–272.
Salmon, W.D. Jr., and Daughaday, W.H., 1957, A hormonally controlled serum factor which stimulates sulfate incorporation by cartilagein vivo. J. Lab. Clin. Med., 49: 825–836.
Shainberg, A., Yagil, G., and Yaffe, D., 1971, Alteration of enzymatic activities during muscle differentiation in vitro, Dev. Biol., 25: 1–29.
Simpson, I.A., and Cushman, S.W., 1988, Hormonal regulation of mammalian glucose transport, Annu. Rev. Biochem., 55: 1059–1089.
Sinha, M.K., Buchanan, C. Leggett, N., Martin, L., Khazanie, P.G., DiMarchi, R., Pories, W.J., and Caro, J.F., 1989, Mechanism of IGF-I-stimulated glucose transport in human adipocytes: Demontration of specific IGF-I receptors not involved in stimulation of glucose transport, Diabetes, 38: 1217–1225.
Walker, P.S., Ramlal, T., Sarabia, V., Koivisto, U.-M., Bilan, P.J., Pessin, J.E., and Klip, A., 1990, Glucose transport activity in L6 muscle cells is regulated by the coordinate control of subcellular glucose transproter distribution, biosynthesis and mRNA transcription,J. Biol. Chem.. 265: 1516–1523.
Widdas, W.F., 1988, Old and new concepts of the membrane transport for glucose in cells, Biochim. Biophys. Acta, 947: 385–404.
Yaffe, D., 1968, Retention of differentiation potentialities during prolonged cultivation of myogenic cells, Proc. Natl. Acad. Sci. U.S.A.. 61: 477–483.
Yasumoto, K., Iwami, K., Fushiki, T., and Mitsuda, H., 1978, Purification and enzymatic properties of γ-glutamyl transferase from bovine colostrum, J. Biochem., 84: 1227–1236.
Zapf, J., Hauri, C. Waldvogel, M., and Froesch, E.R., 1986, Acute metabolic effects and half-lives of intravenously administered insulin-like growth factors I and II in normal and hypophysectomized rats, J. Clin. Invest., 77: 1768–1775.
Zorzano, A., Wilkinson, W., Kotliar, N., Thoidis, G., Wadzinski, B.E., Ruoho, A.E., and Pilch, P.F., 1989, Insulin-regulated glucose uptake in rat adipocytes mediated by two transporter isoforms present in at least two vesicle populations, J. Biol. Chem., 264: 1235–1263.
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 1991 Plenum Press, New York
About this chapter
Cite this chapter
Bilan, P.J., Ramlal, T., Klip, A. (1991). IGF-I Mediated Recruitment of Glucose Transporters from Intracellular Membranes to Plasma Membranes in L6 Muscle Cells. In: Raizada, M.K., LeRoith, D. (eds) Molecular Biology and Physiology of Insulin and Insulin-Like Growth Factors. Advances in Experimental Medicine and Biology, vol 293. Springer, Boston, MA. https://doi.org/10.1007/978-1-4684-5949-4_25
Download citation
DOI: https://doi.org/10.1007/978-1-4684-5949-4_25
Publisher Name: Springer, Boston, MA
Print ISBN: 978-1-4684-5951-7
Online ISBN: 978-1-4684-5949-4
eBook Packages: Springer Book Archive