Influence of Energy Deficiency on the Insulin-like Growth Factor I Axis in a Military Training Program

Abstract

The aim of this study was to determine wether continuous heavy physical activities as well as lack of food and sleep during military training (three weeks of conditioning followed by a five-day combat course) alter serum concentrations of IGF-I and/or its binding proteins, evaluating the relationship to metabolic changes. Before and after training, we measured serum levels of both total and free IGF-I, IGFBP-1 and IGFBP-3 as well as plasma levels of branched-chain amino acids (valine, leucine and isoleucine) and glucose from 26 cadets (21 ± 2 yr). Total and free IGF-I levels were decreased after training from 228 ± 12 to 160 ± 7 ng/ml and from 0.80 ± 0.08 to 0.52 ± 0.06 ng/ml, p < 0.001 respectively) as well as IGFBP-3 (p < 0.001), while IGFBP-1 levels were increased (p < 0.001). BCAA levels were decreased from 245.4 ± 7.5 to 215.9 ± 5.1 µmol/l, p < 0.001, while those of glucose remained unchanged. There were correlations between changes in total IGF-I and IGFBP-3 (p < 0.05) and between free IGF-I and IGFBP-1 (p < 0.01). Several correlations appeared between changes in all the components of the IGF-I axis and branched-chain amino acids. We concluded that responses of the IGF-I system during an intense training could represent an adaptative response to the encountered energy deficiency, resulting a diversion of substrate from growth to acute metabolic needs.

Key words

Intense training · IGF-I · IGFBP-1 · IGFBP-3 · Metabolic parameters

References

• 1 Guezennec C Y, Serrurier B, Aymonod M, Merino D, Pesquies P C. Metabolic and hormonal response to short-term fasting after endurance training in the rat.  Horm Metabol Res. 1984;  16 572-575
• 2 Guezennec C Y, Satabin P, Legrand H, Bigard A X. Physical performance and metabolic changes induced by combined prolonged exercise and different energy intakes in humans.  Eur J Appl Physiol. 1994;  68 525-530
• 3 Bigard A X, Lavier P, Ullman L, Legrand H, Douce P, Guezennec C Y. Branched-chain amino acid supplementation during repeated prolonged skiing exercises at altitude.  Int J Sport Nutr. 1996;  6 295-306
• 4 Opstad P K. Alterations in the morning plasma levels of hormones and the endocrine responses to bicycle exercise during prolonged strain. The significance of energy and sleep deprivation.  Acta Endocrinol. 1991;  125 14-22
• 5 Friedl K E, Moore R J, Hoyt R W, Marchitelli L J, Martinez-Lopez L E, Askew E W. Endocrine markers of semistarvation in healthy lean men in a multistressor environment.  J Appl Physiol. 2000;  88 1820-1830
• 6 Rechler M M, Nissley S P. Peptide growth factors and their receptors. In: Sporn MB, Robert AB (eds) Insulin-like growth factors. Handbook of Pharmacology. Heideberg, Germany; Springer 1990: 263-267
• 7 Rajaman S, Baylink D J, Mohan S. Insulin-like growth factor-binding proteins in serum and other biological fluids: regulation and functions.  Endocrinol Rev. 1997;  18 801-831
• 8 Brausewetter F, Jehle P M, Jung M F, Boehm B O, Brueckel J, Hombach V, Osterhues H H. Microvascular permeability is increased in both types of diabetes and correlates differentially with serum levels of insulin-like growth factor I (IGF-I) and vascular endothelial growth factor (VEGF).  Horm Metab Res. 2001;  33 713-720
• 9 Lee P DK, Conover C A, Powell D R. Regulation and function of insulin-like growth factor binding protein-1.  Proc Soc Exp Biol Med. 1993;  204 4-29
• 10 Lewitt M S, Denyer G S, Cooney G J, Baxter R C. Insulin-like growth factor-binding protein-1 modulates blood glucose levels.  Endocrinol. 1991;  129 2254-2256
• 11 Smith W J, Underwood L E, Clemmons D R. Effects of caloric or protein restriction on insulin-like growth factor I (IGF-I) and IGF-binding proteins in children and adults.  J Clin Endocrinol Metab. 1995;  80 (2) 443-449
• 12 Chicharro J L, Lopez-Calderon C, Hoyos J, Martin-Velasco A I, Villa G, Villañua M A, Lucia A. Effects of an endurance cycling competition on resting serum insulin-like growth factor I (IGF-I) and its binding proteins IGFBP-1 and IGFBP-3.  Br J Sports Med. 2001;  35 303-307
• 13 Eliakim A, Nemet D, Bar-Sela S, Higer Y, Falk B. Changes in circulating IGF-I and their correlation with self-assessment and fitness among elite athletes.  Int J Sports Med. 2002;  23 600-603
• 14 Rosendal L, Landberg H, Flyvbjerg A, Frystyk J, Orskov H, Kjaer M. Physical capacity influences the response of insulin-like growth factor and its binding proteins to training.  J Appl Physiol. 2002;  93 (5) 1669-1675
• 15 Guezennec C Y, Satabin P, Legrand H, Serrurier B, Merino D. Rôle de l’apport calorique sur la capacité à réaliser des efforts physiques et soutenus. Rapport C.E.R.M.A. 87 - 32 (L.C.B.A). December 1987
• 16 Early R J. Capillary gas chromatographic analysis of amino acids in blood and protein hydrolysates as ter-butyldimethylsilyl derivatives.  J Chromato. 1987;  416 15-23
• 17 Gomez-Merino D, Chennaoui M, Drogou C, Bonneau D, Guezennec C Y. Decrease in serum leptin after prolonged physical activity in men.  Med Sci Sports Exerc. 2002;  34 (10) 1594-1599
• 18 Dohm G L, Tapscott E B, Kasperek G J. Protein degradation during endurance exercise and recovery.  Med Sci Sports Exerc. 1987;  19 166-171
• 19 Boulware S D, Tamborlane W V, Rennert N J, Gesundheit N, Sherwin R D. Comparison of the metabolic effects of recombinant human insulin-like growth factor-I and insulin: dose-response relationships in healthy young and middle aged adults.  J Clin Invest. 1994;  93 1131-1139
• 20 Maiter D, Underwood L E, Maes M, Davenport M L, Ketelslegers J M. Different effects of intermittent and continuous growth hormone (GH) administration on serum somatomedin-C/insulin-like growth factor I and liver GH receptors in hypophysectomized rats.  Endocrinology. 1988;  123 1053-1059
• 21 Dall R, Lange K HW, Kjaer M, Jørgensen J OL, Christiansen J S, Ørskov H, Flyvbjerg A. No evidence of insulin-like growth factor-binding protein 3 proteolysis during a maximal exercise test in elite athletes.  J Clin Endocrinol Metab. 2001;  86 (2) 669-674
• 22 Nguyen U N, Mougin F, Simon-Rigaud M L, Rouillon J D, Marguet P, Regnard J. Influence of exercise duration on serum insulin-like growth factor and its binding proteins in athletes.  Eur J Appl Physiol. 1998;  78 533-537
• 23 Zamboni G, Dufillot D, Antoniazzi F, Valentini R, Gendrel D, Tato L. Growth hormone-binding proteins and insulin-like growth factor-binding proteins in protein-energy malnutrition, before and after nutritional rehabilitation.  Pediatr Res. 1996;  3 (3) 410-414
• 24 Eliakim A, Brasel J A, Mohan S, Wong W LT, Cooper D M. Increased physical activity and the growth hormone-IGF-I axis in adolescent males.  Am J Physiol Endocrinol Metab. 1998;  44 R308-R314
• 25 Nemet D, Connolly P H, Pontello-Pescatello A M, Rose-Gottrom C, Larson J K, Galassetti P, Cooper D M. Negative energy balance plays a major role in the IGF-I response to exercise training.  J Appl Physiol. 2004;  96 276-282
• 26 Frystyk J, Ivarsen P, Skjaerbaeck C, Flyvbjerg A, Pedersen E B, Ørskov H. Serum-free insulin-like growth factor I correlates with clearance in patients with chronic renal failure.  Kidney Int. 1999;  56 2076-2084
• 27 Lavoie J M, Fillion Y, Couturier K, Corriveau P. Evidence that the decrease in liver glycogen is associated with the exercise-induced increase in IGFBP-1.  J Appl Physiol. 2002;  93 798-804
• 28 Jousse C, Bruhat A, Ferrara M, Fafournoux P. Physiological concentration of amino acids regulates insulin-like-growth-factor-binding protein 1 expression.  Biochem J. 1998;  334 147-153