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Influence of low- and high-protein diets on insulin and insulin-like growth factor-1 binding to skeletal muscle and liver in the growing rat

Published online by Cambridge University Press:  09 March 2007

D. Dardevet ,
M. Manin ,
M. Balage ,
C. Sornet  and
J. Grizard
D. Dardevet
Affiliation:
INRA Theix, Laboratoire d'Etude du Metabolisme Azoté, 63122 Ceyrat, France
M. Manin
Affiliation:
INRA Theix, Laboratoire d'Etude du Metabolisme Azoté, 63122 Ceyrat, France
M. Balage
Affiliation:
INRA Theix, Laboratoire d'Etude du Metabolisme Azoté, 63122 Ceyrat, France
C. Sornet
Affiliation:
INRA Theix, Laboratoire d'Etude du Metabolisme Azoté, 63122 Ceyrat, France
J. Grizard
Affiliation:
INRA Theix, Laboratoire d'Etude du Metabolisme Azoté, 63122 Ceyrat, France
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Abstract

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The influence of protein content of the diet on the plasma concentrations and binding to skeletal muscle and liver of insulin and insulin-like growth factor-1 (IGF-1), was studied in growing rats. Animals with a starting body-weight of 80 g received for an 11 d period isoenergetic diets containing (g/kg dry matter) 155 protein as controls (MP), or 55 (LP) or 300 (HP) protein. Food was offered as six equal meals/d. Daily food intakes provided adequate amounts of energy. Total plasma IGF-1 increased linearly as a function of dietary protein intake. Plasma insulin was lower in the LP than in the MP and HP groups. Hormone binding was studied in wheat-germ agglutinin (WGA) partially purified skeletal muscle receptor preparations. Each 125I-labelled hormone binding was competed for by increasing amounts of homologous and heterologous unlabelled hormone; this displacement needed lower concentrations of homologous than heterologous hormone. When compared with MP-diet feeding, the LP diet resulted in an increased ligand concentration for half-maximal binding. In addition the specific 125I-labelled insulin and 125I-labelled IGF-1 binding increased at all hormone concentrations and, as revealed by Scatchard analysis, the hormone binding capacity also rose (only significant for low-affinity insulin receptors and high-affinity IGF-1 receptors). The HP diet had little effect on hormone binding, except to increase insulin binding at very low insulin concentrations. Hormone binding was further studied in WGA partially purified liver receptor preparations. Those preparations did not exhibit any detectable specific 125I-labelled IGF-1 binding. The specific 125I-labelled insulin binding was not altered by dietary protein level. It is concluded that the increase in skeletal muscle insulin and IGF-1 binding along with a decrease in insulin and IGF-1 in the blood from rats fed on the LP diet, is consistent with the concept of an inverse relationship between plasma hormone and hormone binding. The physiological significance with respect to metabolic adaptation of muscle remains to be established

Keywords

Dietary proteinInsulin-like growth factor-1Rat
Type
Protein Metabolism
Information
British Journal of Nutrition , Volume 65 , Issue 1 , January 1991 , pp. 47 - 60
Copyright
Copyright © The Nutrition Society 1991

References

REFERENCES

Ablett, R. F., Taylor, M. J. & Selivonchick, D. P. (1983). The effect of high-protein and high-carbohydrate diets on [125I]iodoinsulin binding in skeletal muscle plasma membranes and isolated hepatocytes of rainbow trout (Salmo gairdneri). British Journal of Nutrition 50, 129–139.CrossRefGoogle ScholarPubMed
Adamo, M., Le Roith, D., Simon, J. & Roth, J. (1988). Effect of altered nutritional states on insulin receptors. Annual Review of Nutrition 8, 149–166.CrossRefGoogle ScholarPubMed
Armstrong, D. G., McKay, C. O., Morell, C. & Goddard, C. (1989). Insulin-like growth factor-I binding proteins in serum from the domestic fowl. Journal of Endocrinology 120, 373–378.CrossRefGoogle ScholarPubMed
Balage, M., Grizard, J. & Manin, M. (1990). Effect of calorie restriction on skeletal muscle and liver insulin binding in growing rat. Hormone and Metabolic Research 22, 207–214.CrossRefGoogle ScholarPubMed
Baxter, R. C., Bryson, J. M. & Turtle, J. R. (1980). Somatogenic receptors of rat liver: regulation by insulin. Endocrinology 107, 1176–1181.CrossRefGoogle ScholarPubMed
Baxter, R. C. & Martin, J. L. (1987). Binding proteins for insulin-like growth factors in adult rat serum. Comparison with other human and rat-binding proteins. Biochemical and Biophysical Research Communications 147, 408–415.CrossRefGoogle ScholarPubMed
Bequinot, F., Kahn, R. C., Moses, A. C. & Smith, R. J. (1985). Distinct biologically active receptors for insulin, insulin-like growth factor I, and insulin-like growth factor II in cultured skeletal muscle cells. Journal of Biological Chemistry 260, 15892–15898.CrossRefGoogle Scholar
Bradford, M. (1976). A rapid and sensitive method for quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Chemistry 72, 248–254.Google ScholarPubMed
Burant, C. F., Treutelaar, M. K., Allen, K. D., Sens, D. A. & Buse, M. G. (1987). Comparison of insulin and insulin-like growth factor I-receptors from rat skeletal muscle and L6 myocytes. Biochemical and Biophysical Research Communications 147, 100–107.CrossRefGoogle Scholar
Burant, C. F., Treutelaar, M. K., Block, N. E. & Buse, M. G. (1986). Structural differences between liver- and muscle-derived insulin receptors in rats. Journal of Biological Chemistry 261, 14361–14364.CrossRefGoogle ScholarPubMed
Dollet, J. M., Beck, B., Villaume, C., Max, J. P. & Debry, G. (1985). Progressive adaptation of the endocrine pancreas during long-term protein deficiency in rats: effects on blood glucose homeostasis and pancreatic insulin, glucagon and somatostatin concentrations. Journal of Nutrition 115, 1581–1588.CrossRefGoogle ScholarPubMed
Edozien, J. C., Niehaus, N., Mar, M. H., Makoui, T. & Switzer, B. R. (1978). Diet-hormone interrelationships in the rat. Journal of Nutrition 108, 1767–1776.CrossRefGoogle ScholarPubMed
Florini, J. R. (1987). Hormonal control of muscle growth. Muscle and Nerve 10, 577–598.CrossRefGoogle ScholarPubMed
Fukagawa, N. K., Minaker, K. L., Rowe, J. W., Goodman, M. N., Matthews, D. E., Bier, D. M. & Young, V. R. (1985). Insulin-mediated reduction of whole body protein breakdown. Journal of Clinical Investigation 76, 2306–2311.CrossRefGoogle ScholarPubMed
Garlick, P. J. & Grant, I. (1988). Amino acid infusion increases the sensitivity of muscle protein synthesis in vivo to insulin. Effect of branched-chain amino acids. Biochemical Journal 254, 579–584.CrossRefGoogle ScholarPubMed
Gill, R. D. & Hart, I. C. (1981). Insulin and glucagon binding to hepatocytes in relation to circulating hormones and metabolites in goats maintained on different diets. Hormone and Metabolic Research 13, 603–609.CrossRefGoogle ScholarPubMed
Gourmelen, M., Hossenlopp, P., Cabrol, S., Saab, C., Girard, F. & Binoux, M. (1988). Profil électrophorétique des protéines liantes des IGF (IGF-BP) dans des situations de déséquilibre nutritionnel (Electrophoretic profiles of insulin-like growth factor binding proteins in altered nutritional states). Annales d' Endocrinologie 49, 49C.Google Scholar
Grizard, J. (1983). Insulin binding to skeletal muscle membranes in growing ruminating sheep fed different diets. Reproduction, Nutrition, Développement 23, 389–401.CrossRefGoogle ScholarPubMed
Grizard, J., Prugnaud, J., Arnal, M. & Pion, R. (1975). Effect de I'insuline sur la composition corporelle et les teneurs en acides aminés libres du sang, du foie et du muscle du rat en croissance soumis à une restriction énergétique (Effect of insulin on body composition and free amino acid levels in blood, liver and muscle of the growing rat subjected to energetic restriction). Annales de Biologie Animale, Biochimie, Biophysique 15, 569–582.CrossRefGoogle Scholar
Grizard, J. & Szczygiel, M. (1983). Insulin binding to liver plasma membranes from growing ruminating sheep maintained on different diets. Hormone and Metabolic Research 15, 475–481.CrossRefGoogle ScholarPubMed
Hardouin, S., Hossenlopp, P., Segovia, B., Seurin, D., Portolan, G., Lassarre, C. & Binoux, M. (1987). Heterogeneity of insulin-like growth factor binding proteins and relationships between structure and affinity. I. Circulating forms in man. European Journal of Biochemistry 170, 121–132.CrossRefGoogle ScholarPubMed
Hedo, J. A., Harrison, L. C. & Roth, J. (1981). Binding of insulin receptors to lectins; evidence for common carbohydrate determinants on several membrane receptors. Biochemistry 20, 3385–3393.CrossRefGoogle ScholarPubMed
Hossenlopp, P., Seurin, D., Segovia, B., Portolan, G. & Binoux, M. (1987). Heterogeneity of insulin-like growth factor binding proteins and relationships between structure and affinity. 2. Forms released by human and rat liver in culture. European Journal of Biochemistry 170, 133–142.CrossRefGoogle Scholar
James, D. E., Zorzano, A., Boni-Schnetzler, M., Nemenoff, R. A., Powers, A., Pilch, P. F. & Ruderman, N. B. (1986). Intrinsic differences of insulin receptor kinase activity in red and white muscle. Journal of Biological Chemistry 261, 14939–14944.CrossRefGoogle ScholarPubMed
Jepson, M. M., Bates, P. C. & Millward, D. J. (1988). The role of insulin and thyroid hormones in the regulation of muscle growth and protein turnover in response to dietary protein in the rat. British Journal of Nutrition 59, 397–415.Google ScholarPubMed
Jonas, H. A. (1988). Heterogeneity of receptors for insulin and insulin-like growth factor 1: evidence for receptor subtypes. In Receptor Biochemistry & Methodology, vol. 12B, pp. 19–36 [Kahn, C. R. and Harrison, C., editors]. New York: Alan R. Liss.Google Scholar
Kahn, C. R., Freychet, P., Roth, J. & Neville, D. M. (1974). Quantitative aspects in the insulin-receptors interaction in liver plasma membranes. Journal of Biological Chemistry 249, 2249–2257.CrossRefGoogle ScholarPubMed
Kull, F. C., Jacobs, S., Su, Y. F., Svoboda, M. E., Van Wyk, J. J. & Cuatrecasas, P. (1983). Monoclonal antibodies to receptors for insulin and somatomedin C. Journal of Biological Chemistry 258, 6561–6566.CrossRefGoogle ScholarPubMed
Lopez, S. & Desbuquois, B. (1987). Insulin-related changes in the subcellular distribution of insulin receptors in intact rat liver: effect of acute hypoinsulinemia induced by diazoxide, somatostatin and xylazine. Endocrinology 120, 1695–1702.CrossRefGoogle ScholarPubMed
Lowe, W. L., Adamo, M., Werner, H., Roberts, C. T. & Leroïth, D. (1989). Regulation by fasting of rat insulin-like growth factor I and its receptor. Effect on gene expression and binding. Journal of Clinical Investigation 84, 619–626.CrossRefGoogle ScholarPubMed
Maiter, D., Fliesen, T., Underwood, L. E., Maes, G., Gerard, G., Davenport, M. L. & Ketelslegers, J. M. (1989). Dietary protein restriction decreases insulin-like growth factor I independent of insulin and liver growth hormone binding. Endocrinology 124, 2604–2611.CrossRefGoogle ScholarPubMed
Manin, M., Mizrahi, M., Vye, P., Balage, M. & Grizard, J. (1987). The influence of acute hyperinsulinemia in the insulin-related material in brain, testis, liver and kidney. Metabolism 36, 1067–1072.CrossRefGoogle ScholarPubMed
Okitolonda, W., Brichard, S. M., Pottier, A. M. & Henquin, J. C. (1988). Influence of low- and high-protein diets on glucose homeostasis in the rat. British Journal of Nutrition 60, 509–516.CrossRefGoogle ScholarPubMed
Phillips, L. S. (1986). Nutrition, somatomedins and the brain. Metabolism 35, 78–87.CrossRefGoogle ScholarPubMed
Phillips, L. S., Orawski, A. T. & Belosky, D. C. (1978). Somatomedin and nutrition. IV. Regulation of somatomedin activity and growth cartilage activity by quantity and composition of diet in rats. Endocrinology 103, 121–127.CrossRefGoogle ScholarPubMed
Phillips, L. S. & Scholz, T. D. (1982). Nutrition and somatomedin. IX. Blunting of insulin-like activity by inhibitor in diabetic rat serum. Diabetes 31, 97–104.CrossRefGoogle ScholarPubMed
Prewitt, T. E., D'Ercole, A. J., Switzer, B. R. & Van Wyk, J. J. (1982). Relationship of serum immunoreactive somatomedin C to dietary protein and energy in growing rats. Journal of Nutrition 112, 144–150.CrossRefGoogle ScholarPubMed
Rechler, M. M. & Nissley, S. P. (1985). The nature and regulation of the receptors for insulin-like growth factors. Annual Review of Physiology 47, 425–442.CrossRefGoogle ScholarPubMed
Rosenfeld, R. G. & Dollar, L. A. (1982). Characterization of the somatomedin C/insulin-like growth factor I (SM-C/IGF-1) receptor on cultured human fibroblast monolayers: regulation of receptor concentrations by SM-C/IGF-1 and insulin. Journal of Clinical Endocrinology and Metabolism 55, 434–440.CrossRefGoogle Scholar
Snedecor, G. W. & Cochran, W. G. (1971). Statistical Methods. Ames, Iowa: Iowa State University Press.Google Scholar
Soll, A. H., Kahn, C. R., Neville, D. M. & Roth, J. (1975). Insulin receptor deficiency in genetic and acquired obesity. Journal of Clinical Investigation 56, 769–780.CrossRefGoogle Scholar
Steele, N. C., Rosebrough, R. W., McMurtry, J. P. & Frobish, L. T. (1981). Hepatic insulin receptor characteristics as affected by dietary protein status in swine. Journal of Animal Science 53, Suppl. 1, 265–266.Google Scholar
Stuart, C. A., Pietrzyk, R., Siu, A. K. Q. & Furlanetto, R. W. (1984). Size discrepancy between somatomedin-C and insulin receptors. Journal of Clinical Endocrinology and Metabolism 58, 1–5.CrossRefGoogle ScholarPubMed
Suikkari, A. M., Koivisto, V. A., Rutanen, E. M., Yki-Jarvinen, H., Karonen, S. L. & Sepalla, M. (1988). Prolonged exercise increases serum insulin-like growth factor-binding protein concentrations. Journal of Clinical Endocrinology and Metabolism 66, 266–272.CrossRefGoogle Scholar
Tollefsen, S. E., Thompson, K. & Petersen, D. J. (1987). Separation of the high affinity insulin-like growth factor I receptor from low affinity binding sites by affinity chromatography. Journal of Biological Chemistry 262, 16461–16469.CrossRefGoogle ScholarPubMed
Turner, M. R. (1978). Effect of age and diet on hormone function. Proceedings of the Nutrition Society 37, 295–299.CrossRefGoogle ScholarPubMed
Wang, C., Goldfine, I. D., Fujita-Yamaguchi, Y., Gattner, H. G., Brandenburg, D. & De Meyts, P. (1988). Negative and positive site-site interactions and their modulation by pH, insulin analogs, and monoclonal antibodies, are preserved in the purified insulin receptor. Proceedings of the National Academy of Sciences, USA 85, 8400–8404.CrossRefGoogle ScholarPubMed
Whitehead, R. G. & Lunn, P. G. (1979). Endocrines in protein-energy malnutrition. Proceedings of the Nutrition Society 38, 69–76.CrossRefGoogle ScholarPubMed
Yahya, Z. A. H., Bates, P. C., Dalas, S. S., Morell, D., Holder, A. T., Taylor, A. & Millward, D. J. (1986). The effect of dietary protein concentration on bone and muscle growth and immunoreactive somatomedin C in the rat. Proceedings of the Nutrition Society 45, 107A.Google Scholar
Zorzano, A., James, D. E., Ruderman, N. B. & Pilch, P. F. (1988). Insulin-like growth factor I binding and receptor kinase in red and white muscle. FEBS Letters 234, 257–262.CrossRefGoogle ScholarPubMed