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Insulin-like growth factor-I, but not growth hormone, is dependent on a high protein intake to increase nitrogen balance in the rat

Published online by Cambridge University Press:  09 March 2007

Myriam Sanchez-Gomez ,
Kjell Malmlöf ,
Wilson Mejia ,
Antonio Bermudez ,
Maria Teresa Ochoa ,
Stella Carrasco-Rodriguez  and
Anna Skottner
Myriam Sanchez-Gomez
Affiliation:
Department de Chemistry, Universidad Nacional de Colombia, Santafé de Bogotá, Colombia
Kjell Malmlöf*
Affiliation:
Department of Pharmacology, Peptide Hormones, Pharmacia, Stockholm, Sweden
Wilson Mejia
Affiliation:
Department de Chemistry, Universidad Nacional de Colombia, Santafé de Bogotá, Colombia
Antonio Bermudez
Affiliation:
Department de Chemistry, Universidad Nacional de Colombia, Santafé de Bogotá, Colombia
Maria Teresa Ochoa
Affiliation:
Department de Chemistry, Universidad Nacional de Colombia, Santafé de Bogotá, Colombia
Stella Carrasco-Rodriguez
Affiliation:
Department de Chemistry, Universidad Nacional de Colombia, Santafé de Bogotá, Colombia
Anna Skottner
Affiliation:
Department of Pharmacology, Peptide Hormones, Pharmacia, Stockholm, Sweden
*
*Corresponding author: Dr Kjell Malmlöf, present address Novo Nordisk A/S, GH Biology, Niels Steensens Vej 8, 2820 Gentofte, Denmark, fax +45 44 43 80 06, email [email protected]
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Abstract

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The aim of the present study was to investigate the influence of dietary protein level on the protein anabolic effects of growth hormone (GH) and insulin-like growth factor-I (IGF-I). Female growing rats were fed on either a high- or a low-protein diet with crude protein contents of 222 and 83 g/kg respectively. The diets contained the same amount of metabolizable energy (15·1 MJ/kg) and were given during a 14 d period. During the same time, three groups of rats (n 8) on each diet received subcutaneous infusions of either saline, recombinant human GH (rhGH) or recombinant human IGF-I (rhIGF-I). rhGH and rhIGF-I were given in doses of 360 and 500 μg/d respectively. The low-protein diet alone reduced significantly (P < 0·05) IGF-I concentrations in serum and in tissue taken from the gastrocnemius muscle as well as IGF-I mRNA from the same muscle. The responses to rhGH and rhIGF-I in terms of muscle IGF-I and its mRNA were variable. However, when rhIGF-I was infused into rats on the high-protein diet, significantly elevated levels of IGF-I in muscle tissues could be observed. This was associated with a significantly (P < 0·05) increased N balance, whereas rhGH significantly (P < 0·05) enhanced the N balance in rats on the low-protein diet. Thus, it can be concluded that the level of dietary protein ingested regulates not only the effect of IGF-I on whole-body N economy but also the regulation of IGF-I gene expression in muscles. The exact mechanism by which GH exerts its protein anabolic effect, however, remains to be elucidated.

Keywords

Dietary proteinGrowth hormoneInsulin-like growth factorNitrogen balance
Type
Research Article
Information
British Journal of Nutrition , Volume 81 , Issue 2 , February 1999 , pp. 145 - 152
Copyright
Copyright © The Nutrition Society 1999

References

Bang, P, Eriksson, U, Sara, V, Wivall, I-L & Hall, K (1991) Comparison of acid ethanol extraction and acid gel filtration prior to IGF-I and IGF-II radioimmunoassays. Improvement of determination in acid ethanol extracts by the use of truncated IGF-I as radioligand. Acta Endocrinologica 124, 620–629.Google ScholarPubMed
Behringer, RR, Lewin, TM, Quaife, CJ, Palmiter, RD, Brinster, RL & D'Ercole, AJ (1990) Expression of insulin-like growth factor I stimulates normal somatic growth in growth-hormone deficient transgenic mice. Endocrinology 127, 1033–1040.CrossRefGoogle ScholarPubMed
Bolze, MS, Osborne, JM, Vecbastiks, KA & White, ME (1991) Insulin-like growth factor binding proteins in rats respond to fasting and the protein and energy content of the re-feeding diet. Journal of Nutritional Biochemistry 2, 623–628.Google Scholar
Breier, BH, Bass, JJ, Butler, JH & Gluckman, PD (1986) The somatotrophic axis in young steers: influence of nutritional status on pulsatile release of growth hormone and circulating concentrations of insulin-like growth factor-I. Journal of Endocrinology 111, 209–215.CrossRefGoogle Scholar
Campbell, RG, Johnson, RJ, King, RH, Taverner, MR & Meisinger, DJ (1990) Interaction of dietary protein content and exogenous porcine growth hormone administration on protein and lipid accretion rates in growing pigs. Journal of Animal Science 68, 3217–3225.CrossRefGoogle ScholarPubMed
Clemmons, DR, Smith-Banks, A & Underwood, LE (1992) Reversal of diet-induced catabolism by infusion of recombinant insulin-like growth factor-I in humans. Journal of Clinical Endocrinology and Metabolism 75, 234–238.Google ScholarPubMed
Clemmons, DR & Underwood, LE (1991) Nutritional regulation of IGF-I and IGF-I binding proteins. Annual Review of Nutrition 11, 393–412.CrossRefGoogle Scholar
Dardevet, D, Manin, M, Sornet, C, Attaix, D, Baracos, VE & Grizard, J (1994) Insulin-like growth factor-I and insulin resistance in skeletal muscles of adult and old rats. Endocrinology 134, 1475–1484.CrossRefGoogle ScholarPubMed
Daughaday, WH, Mariz, IK & Bleten, SL (1980) Inhibition of access of bound somatomedin to membrane receptor and immunobinding sites: a comparison of radioreceptor and radioimmunoassay of somatomedin in native and acid–ethanol-extracted serum. Journal of Clinical Endocrinology and Metabolism 51, 781–788.CrossRefGoogle Scholar
Daughaday, WH & Rotwein, P (1989) Insulin-like growth factors I and II. Peptide, messenger ribonucleic acid and gene structures, serum and tissue concentrations. Endocrine Reviews 10, 68–91.CrossRefGoogle ScholarPubMed
Dodson, MW, Allen, RE & Hossner, KL (1985) Ovine somatomedin multiplication - stimulating activity and insulin promote skeletal muscle satellite cell proliferation in vitro. Endocrinology 117, 2357–2363.CrossRefGoogle ScholarPubMed
Douglas, RG, Gluckman, PD, Ball, K, Breier, B & Shaw, JH (1991) The effects of infusion of insulin-like growth factor (IGF)-I, IGF-II, and insulin on glucose and protein metabolism in fasted lambs. Journal of Clinical Investigation 88, 614–622.CrossRefGoogle ScholarPubMed
Durnam, DM & Palmiter, RD (1983) A practical approach for quantitating specific mRNAs by solution hybridization. Analytical Biochemistry 131, 385–393.CrossRefGoogle ScholarPubMed
Eriksson, S, Sanne, S & Thomke, S (1976) Fodermedelstabeller och ut-fodringsrekomendationer (Feed tables and feeding recommendations), pp. 36–41. Borås: LTs förlag.Google Scholar
Fryburg, DA, Gelfand, RA & Barrett, EJ (1991) Growth hormone acutely stimulates forearm muscle protein synthesis in normal humans. American Journal of Physiology 260, E499–E504.Google ScholarPubMed
Gelfand, RA & Barrett, EJ (1987) Effect of physiological hyperinsulinemia on skeletal muscle protein synthesis and breakdown in man. Journal of Clinical Investigation 80, 1–6.CrossRefGoogle ScholarPubMed
Grant, AL, Helferich, WG, Kramer, SA, Merkel, RA & Bergen, WG (1991) Administration of growth hormone to pigs alters the relative amount of insulin-like growth factor-I mRNA in liver and skeletal muscle. Journal of Endocrinology 130, 331–338.CrossRefGoogle ScholarPubMed
Grimble, GK, West, MF, Acuti, AB, Rees, RG, Hunjan, MK, Webster, JD, Frost, PG & Silk, DB (1988) Assessment of an automated chemiluminescence nitrogen analyzer for routine use in clinical nutrition. Journal of Parenteral and Enteral Nutrition 12, 100–106.CrossRefGoogle ScholarPubMed
Harp, JB, Goldstein, S & Phillips, LS (1991) Nutrition and somatomedin. XXIII. Molecular regulation of IGF-I by amino acid availability in cultured hepatocytes. Diabetes 40, 95–101.CrossRefGoogle ScholarPubMed
Hayden, JM, Marten, NW, Burke, EJ & Straus, DS (1994) The effect of fasting on insulin-like growth factor-I nuclear transcript abundance in rat liver. Endocrinology 134, 760–768.CrossRefGoogle ScholarPubMed
Hizuka, N, Takano, K, Shizume, K, Asakawa, K, Miyakawa, M, Tanaka, Y & Horikawa, R (1986) Insulin-like growth factor-I stimulates growth in normal growing rats. European Journal of Pharmacology 125, 143–146.CrossRefGoogle ScholarPubMed
Isgaard, J, Nilsson, A, Vikman, K & Isaksson, OGP (1989) Growth hormone regulates the level of insulin-like growth factor-I mRNA in rat skeletal muscle. Journal of Endocrinology 120, 107–112.CrossRefGoogle ScholarPubMed
Labarca, C & Paigen, K (1980) A simple, rapid and sensitive DNA assay procedure. Analytical Biochemistry 102, 344–352.CrossRefGoogle ScholarPubMed
MacRae, JC, Bruce, LA, Hovell, FD, DeB Hart, IC, Inkster, J, Walker, A & Atkinson, T (1991) Influence of protein nutrition on the response of growing lambs to exogenous bovine growth hormone. Journal of Endocrinology 130, 53–61.CrossRefGoogle ScholarPubMed
Maes, M, Amand, Y, Underwood, LE, Maiter, D & Ketelslegers, JM (1988) Decreased serum insulin-like growth factor I response to growth hormone in hypophysectomized rats fed a low protein diet: evidence for a postreceptor defect. Acta Endocrinologica 117, 320–326.Google ScholarPubMed
Malmlöf, K, Cortova, Z, Saxerholt, H, Karlsson, E, Arrhenius-Nyberg, V & Skottner, A (1995) Effects of insulin-like growth factor-I and growth hormone on the net flux of amino acids across the hind limbs in the surgically traumatized pig. Clinical Science 88, 285–292.CrossRefGoogle ScholarPubMed
Mathews, LS, Norstedt, G & Palmiter, RD (1986) Regulation of insulin-like growth factor I gene expression by growth hormone. Proceedings of the National Academy of Sciences USA 83, 9343–9347.CrossRefGoogle ScholarPubMed
Möller, C, Arner, P, Sonnenfeld, T & Norstedt, G (1991) Quantitative comparison of insulin-like growth factor mRNA levels in human and rat tissues analysed by a solution hybridization assay. Journal of Molecular Endocrinology 7, 213–222.CrossRefGoogle ScholarPubMed
Nilsson, A, Ohlsson, C, Isaksson, OGP, Lindahl, A & Isgaard, J (1994) Hormonal regulation of longitudinal bone growth. European Journal of Clinical Nutrition 48, S150–S160.Google ScholarPubMed
Okamura, K, Okuma, T, Tabira, Y & Miyauchi, Y (1989) Effect of administered human growth hormone on protein metabolism in septic rats. Journal of Parenteral and Enteral Nutrition 13, 450–454.CrossRefGoogle ScholarPubMed
Pell, JM & Bates, PC (1992) Differential actions of growth hormone and insulin-like growth factor-I on tissue protein catabolism in dwarf mice. Endocrinology 130, 1942–1950.Google ScholarPubMed
Phillips, LS (1986) Nutrition, somatomedins and the brain. Metabolism 35, 78–87.CrossRefGoogle ScholarPubMed
Press, M (1988) Growth hormone and metabolism. Diabetes/ Metabolism Reviews 4, 391–414.CrossRefGoogle ScholarPubMed
SAS Institute Inc. (1985) SAS User's Guide, Statistics, 5th ed. Cary, NC: SAS Institute Inc.Google Scholar
Skottner, A, Clark, RG, Robinson, ICAF & Fryklund, L (1987) Recombinant human insulin-like growth factor: testing the somatomedin hypothesis in hypophysectomized rats. Journal of Endocrinology 112, 123–132.CrossRefGoogle ScholarPubMed
Snyder, DK, Underwood, LE & Clemmons, DR (1990) Anabolic effects of growth hormone in obese diet-restricted subjects are dose dependent. American Journal of Clinical Nutrition 52, 431–437.CrossRefGoogle ScholarPubMed
Straus, DS & Takemoto, CD (1990) Effect of dietary protein deprivation on insulin-like growth factor (IGF)-I and -II, IGF binding protein-2 and serum albumin gene expression in rat. Endocrinology 127, 1849–1860.CrossRefGoogle ScholarPubMed
Takahashi, S, Kajikawa, M, Umezawa, T, Takahashi, S-I, Kato, H, Miura, Y, Nam, TJ, Noguchi, T & Naito, H (1990) Effect of dietary proteins on the plasma immunoreactive insulin-like growth factor-1/somatomedin C concentration in the rat. British Journal of Nutrition 63, 521–534.CrossRefGoogle ScholarPubMed
Thissen, JP, Pucilowska, JB & Underwood, LE (1994) Differential regulation of insulin-like growth factor-I (IGF-I) and IGF binding protein-I messenger ribonucleic acid by amino acid availability and growth hormone in rat hepatocyte primary culture. Endocrinology 134, 1570–1576.CrossRefGoogle Scholar
Thissen, JP, Triest, S, Moats-Staats, BM, Underwood, LE, Mauerhoof, T, Maiter, D & Ketelslegers, JM (1991 a) Evidence that pretranslational and translational defects decrease serum insulin-like growth factor-I concentrations during dietary protein-restriction. Endocrinology 129, 429–435.CrossRefGoogle ScholarPubMed
Thissen, JP, Triest, S, Underwood, LE, Maes, M & Ketelslegers, JM (1990) Divergent responses of serum insulin-like growth factor-I and liver growth hormone (GH) receptors to exogenous GH in protein restricted rats. Endocrinology 126, 908–913.CrossRefGoogle ScholarPubMed
Thissen, JP & Underwood, LE (1992) Translational status of the insulin-like growth factor-I mRNAs in liver of protein-restricted rats. Endocrinology 132, 141–147.CrossRefGoogle ScholarPubMed
Thissen, JP, Underwood, LE, Maiter, D, Maes, M, Clemmons, DR & Ketelslegers, JM (1991 b) Failure of insulin-like growth factor-I infusion to promote growth in protein-restricted rats despite normalization of serum IGF-I concentrations. Endocrinology 128, 885–890.CrossRefGoogle ScholarPubMed
Tomas, FM, Knowles, SE, Chandler, CS, Francis, GL, Owens, PC & Ballard, FJ (1993) Anabolic effects of insulin-like growth factor-I (IGF-I) and IGF-I variant in normal female rats. Journal of Endocrinology 137, 413–421.CrossRefGoogle ScholarPubMed
Tomas, FM, Knowles, SE, Owens, PC, Read, LC, Chandler, CS, Gargosky, SE & Ballard, FJ (1991) Effects of full-length and truncated insulin-like growth factor-I on nitrogen balance and muscle protein metabolism in nitrogen-restricted rats. Journal of Endocrinology 128, 97–105.CrossRefGoogle ScholarPubMed
Ullman, M & Oldfors, A (1989) Effects of growth hormone on skeletal muscle. I. Studies on normal adult rats. Acta Physiologica Scandinavica 135, 531–536.CrossRefGoogle ScholarPubMed
VandeHaar, MJ, Moats-Staats, BM, Davenport, ML, Walker, JL, Ketelslegers, JM, Sharma, BK & Underwood, LE (1991) Reduced serum concentrations of insulin-like growth factor-I (IGF-I) in protein-restricted growing rats is accompanied by reduced IGF-I mRNA levels in liver and skeletal muscle. Journal of Endocrinology 130, 305–312.CrossRefGoogle ScholarPubMed