Abstract
This study investigated the hypothesis that the duration of aerobic-based cycle exercise would affect the adaptations in substrate and metabolic regulation that occur in vastus lateralis in response to a short-term (10 day) training program. Healthy active but untrained males (n = 7) with a peak aerobic power (\( \dot{V}{\text{O}}_{{ 2 {\text{ peak}}}} \)) of 44.4 ± 1.4 ml kg−1 min−1 participated in two different training programs with order randomly assigned (separated by ≥2 weeks). The training programs included exercising at a single intensity designated as light (L) corresponding to 60 % \( \dot{V}{\text{O}}_{{ 2 {\text{ peak}}}} \), for either 30 or 60 min. In response to a standardized task (60 % \( \dot{V}{\text{O}}_{{ 2 {\text{ peak}}}} \)), administered prior to and following each training program, L attenuated the decrease (P < 0.05) in phosphocreatine and the increase (P < 0.05) in free adenosine diphosphate and free adenosine monophosphate but not lactate. These effects were not altered by daily training duration. In the case of muscle glycogen, training for 60 versus 30 min exaggerated the increase (P < 0.05) that occurred, an effect that extended to both rest and exercise concentrations. No changes were observed in \( \dot{V}{\text{O}}_{{ 2 {\text{ peak}}}} \) measured during progressive exercise to fatigue or in \( \dot{V}{\text{O}}_{ 2} \) and RER during submaximal exercise with either training duration. These findings indicate that reductions in metabolic strain, as indicated by a more protected phosphorylation potential, and higher glycogen reserves, can be induced with a training stimulus of light intensity applied for as little as 30 min over 10 days. Our results also indicate that doubling the duration of daily exercise at L although inducing increased muscle glycogen reserves did not result in a greater metabolic adaptation.
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References
Bergström J (1962) Muscle electrolytes in man. Scand J Clin Lab Invest 68:1–110
Burelle Y, Hochachka PW (2002) Endurance training induces muscle-specific changes in mitochrondrial function in skinned muscle fibers. J Appl Physiol 92:2429–2438
Burgomaster KA, Howarth KR, Phillips SM, Rakobowchuck M, MacDonald MJ, McGee SI, Gibala MJ (2008) Similar metabolic adaptations during exercise after low volume sprint interval training and traditional endurance training in humans. J Physiol 586:151–160
Cadefau J, Green HJ, Cussó R, Ball-Burnett M, Jamieson G (1994) Coupling of muscle phosphorylation potential to glycolysis during submaximal exercise of varying intensity following short term training. J Appl Physiol 76:2586–2593
Chesley A, Heigenhauser GF, Spriet LL (1996) Regulation of glycogen phosphorylase activity following short-term endurance training. Am J Physiol 270:E328–E335
Coffey VG, Hawley JA (2007) The molecular basis of training adaptation. Sports Med 37:737–763
Coggan AR, Williams BD (1995) Metabolic adaptations to endurance training: substrate metabolism during exercise. In: Hargreaves M (ed) Exercise metabolism. Human Kinetics Publishers, Inc., Champaign, pp 177–210
Connett RJ, Honig CR, Gayeski TEJ, Brooks GA (1990) Defining hypoxia: a systems view of VO2, glycolysis, energetics and intracellular PO2. J Appl Physiol 68:833–842
Daussin FN, Zoll J, Dufour SP, Ponset E, Lonsdorfer-Wollf E, Doutreleau S, Mettauer B, Piquard F, Geny B, Richard R (2008a) Effect of interval versus continuous training on cardiorespiratory and mitochondrial functions: relationship to aerobic performance improvements in sedentary subjects. Am J Physiol 295:R264–R272
Daussin FN, Zoll J, Ponset E, Dufour S, Doutreleau S, Lonsdorfer E, Ventura-Clapier R, Mettauer B, Piquard F, Geny B, Richard R (2008b) Training at high exercise intensity promotes qualitative adaptations of mitochondrial function in human skeletal muscle. J Appl Physiol 97:104
Duhamel TA, Green HJ, Perco JG, Ouyang J (2006) Effects of prior exercise and a low-carbohydrate diet on muscle sarcoplasmic reticulum function during cycling in women. J Appl Physiol 101:695–706
Egan B, Carson BP, Garcia-Roves PM, Chibalin AV, Sarsfield FM, Barron N, McCaffrey N, Moyna NM, Zierath JR, O’Gorman DJ (2010) Exercise intensity-dependent regulation of peroxisome proliferator-activated receptor γ coactivator-1α mRNA abundance is associated with differential activation of upstream signalling kinases in human skeletal muscle. J Physiol 588:1779–1790
Flück M (2006) Functional, structural and molecular plasticity of mammalian skeletal muscle in response to exercise stimuli. J Exp Biol 209:2239–2248
Gibala MJ, McGee SL (2008) Metabolic adaptations to short-term high-intensity interval training: a little pain for a lot of gain? Exerc Sport Sci Rev 36:58–63
Gibala MJ, Little JP, van Essen M, Wilkin GP, Burgomaster KA, Safdar A, Raha S, Tarnopolsky MA (2006) Short term interval versus traditional endurance training; similar initial adaptations in human skeletal muscle and exercise performance. J Physiol 575(3):901–911
Gladden LB (1996) Lactate transport and exchange during exercise. In: Rowell LB, Shephard RJ (eds) Handbook of physiology, exercise regulation and integration of multiple systems. Oxford University Press, New York, pp 614–648
Gollnick PD, Saltin B (1982) Significance of skeletal muscle oxidative enzyme enhancement with endurance training. Clin Physiol 2:1–12
Gollnick PD, Armstrong RB, Saubert CW IV, Sembrowich WL, Shepherd RE, Saltin B (1973) Glycogen depletion patterns in human skeletal muscle fibres during prolonged work. Pflügers Arch 344:1–12
Grandlun AG, Kotova O, Benziane B, Galuska D, Jensen-Waern M, Chibalin A, Essen-Gustausson B (2010) Effects of exercise on muscle glycogen synthesis signalling and enzyme activities in pigs carrying the PRKAG3 mutation. Exp Physiol 95:541–549
Green HJ, Sutton J, Young P, Cymerman A, Houston CS (1989) Operation everest II: muscle energetics during maximal exhaustive exercise. J Appl Physiol 66:142–150
Green HJ, Smith D, Murphy P, Fraser I (1990) Training-induced alterations in muscle glycogen utilization in fibre-specific types during prolonged exercise. Can J Physiol Pharmacol 68:1372–1376
Green HJ, Jones S, Ball-Burnett ME, Smith D, Livesey J, Farrance BW (1991) Early muscular and metabolic adaptations to prolonged exercise training in man. J Appl Physiol 70:2032–2038
Green H, Helyar R, Ball-Burnett M, Kowalchuk N, Symon S, Farrance B (1992) Metabolic adaptations to training precede changes in muscle mitochondrial capacity. J Appl Physiol 72:484–491
Green HJ, Cadefau J, Cussó R, Ball-Burnett M, Jamieson G (1995) Metabolic adaptations to short term training are expressed early in exercise. Can J Physiol Pharmacol 73:474–482
Green H, Grant S, Bombardier E, Ranney D (1999) Initial aerobic power does not alter muscle metabolic adaptations to short-term training. Am J Physiol 277:E39–E48
Green HJ, Tupling R, Roy B, O’Toole D, Burnett M, Grant S (2000) Adaptations in skeletal muscle exercise metabolism to a sustained session of heavy intermittent exercise. Am J Physiol 278:E118–E126
Green HJ, Bombardier E, Duhamel TA, Stewart RD, Tupling AR, Ouyang J (2008) Metabolic, enzymatic and transporter responses in human muscle to consecutive days of exercise and recovery. Am J Physiol 295:R1238–R1250
Green HJ, Bombardier E, Burnett ME, Smith IC, Tupling SM, Ranney DA (2009a) Time-dependent effects of short-term training on muscle metabolism during the early phase of exercise. Am J Physiol 297:R1383–R1391
Green HJ, Burnett ME, Smith IC, Tupling SM, Ranney DA (2009b) Failure of hypoxia to exaggerate the metabolic stress in working muscle following short-term training. Am J Physiol Regul Integr Comp Physiol 297:R593–R604
Green HJ, Burnett M, Ouyang J, Smith I, Tupling S (2011) Can increases in capillarization explain the early metabolic adaptations in humans to short term training? Can J Physiol Pharmacol (in revision)
Harris RC, Hultman E, Nordesjö L-O (1974) Glycolytic intermediates and high energy phosphates determined in biopsy samples of musculus femoris of man at rest. Scand J Clin Lab Invest 33:102–120
Hochachka PW, Matheson GO (1992) Regulating ATP turnover over broad dynamic work ranges in skeletal muscles. J Appl Physiol 73:1697–1703
Holloszy JO (2003) A forty-year memoir of research on the regulation of glucose transport into muscle. Am J Physiol 284:E453–E467
Holloszy JO, Coyle EF (1984) Adaptations of skeletal muscle to endurance exercise and their metabolic consequences. J Appl Physiol 56:831–838
Hughson RL, Kowalchuk JM, Prime WM, Green HJ (1980) Open-circuit gas exchange analysis in the non-steady state. Can J Appl Sport Sci 5:15–18
Hughson RL, Green HJ, Sharratt MT (1995) Gas exchange, blood lactate and plasma catecholamines during incremental exercise in hypoxia and normoxia. J Appl Physiol 79:1134–1141
Ingebretson DC, Bakken AM, Segadal L, Farstad M (1982) Determination of adenine nucleotides and inosine in human myocardium by ion pair reversed phase high performance liquid chromatography. J Chromatogr 242:119–126
Jensen TE, Wojtaszewski FP, Richter EA (2009) AMP-activated protein kinase in contraction regulation of skeletal muscle metabolism: necessary and/or sufficient? Acta Physiol 196:155–174
Jorgensen SB, Richter EA, Wojtaszewski JFP (2006) Role of AMPK in skeletal muscle metabolic regulation and adaptation in relation to exercise. J Physiol 574:17–31
Klip AK, Schertzer JD, Bilan PJ, Thong F, Antonescu C (2009) Regulation of glucose 4 traffic by energy deprivation from mitochondrial compromise. Acta Physiol Scand 196:27–35
Korzeniewski B (2003) Regulation of oxidative phosphorylation in different muscles and various experimental conditions. Biochem J 375:799–804
Little JP, Safdar AS, Tarnopolsky MA, Gibala MJ (2010) A practical model of low-volume high-intensity interval training induces mitochondrial biogenesis in human skeletal muscle: potential mechanisms. J Physiol 588:1011–1022
Lowry OH, Passonneau JV (1972) A flexible system of enzymatic analysis. Academic Press, New York
McConell GK, Lee-Young RS, Ping-Chen Z, Stepto NK, Huynh NN, Stephens TJ, Canny BJ, Kemp BE (2005) Short-term exercise training in humans reduces AMPK signaling during prolonged exercise independent of muscle glycogen. J Physiol 568:665–678
McKay BR, Paterson DH, Kowalchuk JM (2009) Effect of short-term high intensity interval training versus continuous training on O2 uptake kinetics, muscle deoxygenation and exercise performance. J Appl Physiol 107:128–138
Meyer RA, Foley JM (1996) Cellular processes integrating the metabolic response to exercise. In: Shephard J, Rowell L (eds) Handbook of physiology. Exercise regulation and integration of multiple systems. Oxford University Press, New York, pp 841–869
Murgia MM, Jensen TE, Cusinato M, Garcia M, Richter EA, Schiaffino S (2009) Multiple signalling pathways redundantly control glucose transporter GLUT4 gene transcription in skeletal muscle. J Physiol 587:4319–4327
Phillips SM, Green HJ, MacDonald MJ, Hughson RL (1995a) Progressive effect of endurance training on VO2 kinetics at the onset of submaximal exercise. J Appl Physiol 79:1914–1920
Phillips SM, Green HJ, Tarnopolsky MA, Grant SM (1995b) Decreased glucose turnover following short term training is unaccompanied by changes in muscle oxidation potential. Am J Physiol 269:E222–E230
Phillips SM, Green HJ, Tarnopolsky LJ, Heigenhauser GM, Hill RE, Grant SM (1996a) Effects of training on substrate turnover and oxidation during exercise. J Appl Physiol 81:2182–2191
Phillips SM, Green HJ, Tarnopolsky MA, Heigenhauser GJF, Grant SM (1996b) Progressive effect of endurance training on metabolic adaptations in working skeletal muscle. Am J Physiol 33:E265–E272
Phillips SM, Han X-X, Green HJ, Bonen A (1996c) Increments in skeletal muscle GLUT-1 and GLUT-4 following endurance training in humans. Am J Physiol 270:E456–E462
Putnam CT, Jones NL, Hultman E, Hollidge-Horvat MG, Bonen A, McConachie DR, Heigenhauser GF (1998) Effects of short-term submaximal training in humans on muscle metabolism in exercise. Am J Physiol 275:E132–E139
Rumsey WL, Wilson DF (1996) Tissue capacity for mitochondrial oxidative phosphorylation and its adaptation to stress. In: Fregly MJ, Blatteis CM (eds) Handbook of physiology: environmental physiology. Oxford University Press, New York, pp 1095–1113
Sahlin K, Harris RC, Nylund B, Hultman E (1976) Lactate content and pH in muscle samples obtained after dynamic exercise. Pflügers Arch 367:143–149
Shoemaker JK, Phillips SM, Green HJ, Hughson RL (1996) Faster femoral artery blood velocity kinetics at the onset of exercise following short term training. Cardiovasc Res 31:278–286
Spencer MK, Yan Z, Katz A (1991) Carbohydrate supplementation attenuates IMP accumulation in human muscle during prolonged exercise. Am J Physiol 261:C71–C76
Spencer MK, Yan Z, Katz A (1992) Effect of low glycogen on carbohydrate and energy metabolism in human muscle during exercise. Am J Physiol 262:C975–C979
Spina RJ, Chi MMY, Hopkins MG, Nemeth PM, Lowry OH, Holloszy JO (1996) Mitochondrial enzyme increase in muscle in response to 7–10 days of cycle exercise. J Appl Physiol 80:2250–2254
Tonkonogi M, Sahlin K (2002) Physical exercise and mitochondrial function in human skeletal muscle. Exerc Sport Sci Rev 30:129–137
Tullson PC, Bangsbo J, Hellsten Y, Richter EA (1995) IMP metabolism in human skeletal muscle after exhaustive exercise. J Appl Physiol 78:146–152
Uguccioni G, Hood DA (2010) The importance of PGC-1a in contractile activity-induced mitochondrial adaptations. Am J Physiol 300:E361–E371
Wasserman DH, Cherrington AD (1996) Regulation of extramuscular fuel sources during exercise. In: Rowell LB, Shephard RJ (eds) Handbook of physiology, section 12: exercise, regulation and integration of multiple systems. Oxford University Press, New York, pp 1036–1074
Zoll J (2002) Quantitative and qualitative adaptation of skeletal muscle mitochondria to increased physical activity. J Cell Physiol 194:180–193
Zoll J, Sanchez H, Guessan N, Ribera F, Lampert E, Bigard X, Serrurier B, Fortin D, Geny B, Veksler V, Ventura R (2002) Physical activity changes the rate of mitochondrial respiration in human skeletal muscle. J Physiol 543:191–200
Zwetsloot KA, Westerkamp IM, Holmes BF, Gavin TP (2008) AMPK regulates basal skeletal muscle capillarization and VEGF expression but is not necessary for angiogenic response to exercise. J Physiol 586:6021–6035
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This work was supported by a grant from the Supply and Services Canada and the Civil Institute of Environmental Medicine (DCIEM).
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Communicated by Michael Lindinger.
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Green, H.J., Burnett, M., Jacobs, I. et al. Adaptations in muscle metabolic regulation require only a small dose of aerobic-based exercise. Eur J Appl Physiol 113, 313–324 (2013). https://doi.org/10.1007/s00421-012-2434-5
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DOI: https://doi.org/10.1007/s00421-012-2434-5