Skip to main content

Intramyocellular lipid and glycogen content are reduced following resistance exercise in untrained healthy males

Abstract

Resistance exercise has recently been shown to improve whole-body insulin sensitivity in healthy males. Whether this is accompanied by an exercise-induced decline in skeletal muscle glycogen and/or lipid content remains to be established. In the present study, we determined fibre-type-specific changes in skeletal muscle substrate content following a single resistance exercise session. After an overnight fast, eight untrained healthy lean males participated in a ~45 min resistance exercise session. Muscle biopsies were collected before, following cessation of exercise, and after 30 and 120 min of post-exercise recovery. Subjects remained fasted throughout the test. Conventional light and (immuno)fluorescence microscopy were applied to assess fibre-type-specific changes in intramyocellular triacylglycerol (IMTG) and glycogen content. A significant 27±7% net decline in IMTG content was observed in the type I muscle fibres (P<0.05), with no net changes in the type IIa and IIx fibres. Muscle glycogen content decreased with 23±6, 40±7 and 44±7% in the type I, IIa and IIx muscle fibres, respectively (P<0.05). Fibre-type-specific changes in intramyocellular lipid and/or glycogen content correlated well with muscle fibre-type oxidative capacity. During post-exercise recovery, type I muscle fibre lipid content returned to pre-exercise levels within 120 min. No changes in muscle glycogen content were observed during recovery. We conclude that intramyocellular lipid and glycogen stores are readily used during resistance exercise and this is likely associated with the reported increase in whole-body insulin sensitivity following resistance exercise.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  • Bergstrom J (1975) Percutaneous needle biopsy of skeletal muscle in physiological and clinical research. Scand J Clin Lab Invest 35:609–616

    PubMed  Article  CAS  Google Scholar 

  • Bogardus C, Thuillez P, Ravussin E, Vasquez B, Narimiga M, Azhar S (1983) Effect of muscle glycogen depletion on in vivo insulin action in man. J Clin Invest 72:1605–1610

    PubMed  Article  CAS  Google Scholar 

  • Bruce CR, Kriketos AD, Cooney GJ, Hawley JA (2004) Disassociation of muscle triglyceride content and insulin sensitivity after exercise training in patients with Type 2 diabetes. Diabetologia 47:23–30

    Article  PubMed  CAS  Google Scholar 

  • Chapman J, Garvin AW, Ward A, Cartee GD (2002) Unaltered insulin sensitivity after resistance exercise bout by postmenopausal women. Med Sci Sports Exerc 34:936–941

    Article  PubMed  CAS  Google Scholar 

  • Craig BW, Everhart J, Brown R (1989) The influence of high-resistance training on glucose tolerance in young and elderly subjects. Mech Ageing Dev 49:147–157

    Article  PubMed  CAS  Google Scholar 

  • Derave W, Hansen BF, Lund S, Kristiansen S, Richter EA (2000) Muscle glycogen content affects insulin-stimulated glucose transport and protein kinase B activity. Am J Physiol Endocrinol Metab 279:E947–E955

    PubMed  CAS  Google Scholar 

  • Devlin JT, Horton ES (1985) Effects of prior high-intensity exercise on glucose metabolism in normal and insulin-resistant men. Diabetes 34:973–979

    PubMed  Article  CAS  Google Scholar 

  • Devlin JT, Hirshman M, Horton ED, Horton ES (1987) Enhanced peripheral and splanchnic insulin sensitivity in NIDDM men after single bout of exercise. Diabetes 36:434–439

    PubMed  Article  CAS  Google Scholar 

  • Essen-Gustavsson B, Tesch PA (1990) Glycogen and triglyceride utilization in relation to muscle metabolic characteristics in men performing heavy-resistance exercise. Eur J Appl Physiol Occup Physiol 61:5–10

    Article  PubMed  CAS  Google Scholar 

  • Evans WJ (1995) Effects of exercise on body composition and functional capacity of the elderly. J Gerontol A Biol Sci Med Sci 50 Spec No:147–150

  • Fenicchia LM, Kanaley JA, Azevedo JL Jr, Miller CS, Weinstock RS, Carhart RL, Ploutz-Snyder LL (2004) Influence of resistance exercise training on glucose control in women with type 2 diabetes. Metabolism 53:284–289

    Article  PubMed  CAS  Google Scholar 

  • Fluckey JD, Hickey MS, Brambrink JK, Hart KK, Alexander K, Craig BW (1994) Effects of resistance exercise on glucose tolerance in normal and glucose-intolerant subjects. J Appl Physiol 77:1087–1092

    PubMed  CAS  Google Scholar 

  • Fry AC (2004) The role of resistance exercise intensity on muscle fibre adaptations. Sports Med 34:663–679

    PubMed  Article  Google Scholar 

  • Garcia-Roves PM, Han DH, Song Z, Jones TE, Hucker KA, Holloszy JO (2003) Prevention of glycogen supercompensation prolongs the increase in muscle GLUT4 after exercise. Am J Physiol Endocrinol Metab 285:E729–E736

    PubMed  CAS  Google Scholar 

  • Goodpaster BH, Kelley DE, Wing RR, Meier A, Thaete FL (1999) Effects of weight loss on regional fat distribution and insulin sensitivity in obesity. Diabetes 48:839–847

    PubMed  Article  CAS  Google Scholar 

  • Gosker HR, van Mameren H, van Dijk PJ, Engelen MP, van der Vusse GJ, Wouters EF, Schols AM (2002) Skeletal muscle fibre-type shifting and metabolic profile in patients with chronic obstructive pulmonary disease. Eur Respir J 19:617–625

    Article  PubMed  CAS  Google Scholar 

  • Gutmann I, Wahlefeld AW (1974) L-(+)-Lactate, determination with lactate dehydrogenase and NAD. In: Bergmeyer HU (ed) Methods in enzymatic analysis, 2nd edn. Academic, New York, pp 1464–1468

    Google Scholar 

  • He J, Goodpaster BH, Kelley DE (2004) Effects of weight loss and physical activity on muscle lipid content and droplet size. Obes Res 12:761–769

    PubMed  Article  Google Scholar 

  • Hegarty BD, Furler SM, Ye J, Cooney GJ, Kraegen EW (2003) The role of intramuscular lipid in insulin resistance. Acta Physiol Scand 178:373–383

    Article  PubMed  CAS  Google Scholar 

  • Hoppeler H, Howald H, Conley K, Lindstedt SL, Claassen H, Vock P, Weibel ER (1985) Endurance training in humans: aerobic capacity and structure of skeletal muscle. J Appl Physiol 59:320–327

    PubMed  CAS  Google Scholar 

  • Houmard JA, Tanner CJ, Yu C, Cunningham PG, Pories WJ, MacDonald KG, Shulman GI (2002) Effect of weight loss on insulin sensitivity and intramuscular long-chain fatty acyl-CoAs in morbidly obese subjects. Diabetes 51:2959–2963

    PubMed  Article  CAS  Google Scholar 

  • Howald H, Boesch C, Kreis R, Matter S, Billeter R, Essen-Gustavsson B, Hoppeler H (2002) Content of intramyocellular lipids derived by electron microscopy, biochemical assays, and (1)H-MR spectroscopy. J Appl Physiol 92:2264–2272

    PubMed  CAS  Google Scholar 

  • Kadi F, Thornell LE (2000) Concomitant increases in myonuclear and satellite cell content in female trapezius muscle following strength training. Histochem Cell Biol 113:99–103

    Article  PubMed  CAS  Google Scholar 

  • Keul J, Haralambie G, Bruder M, Gottstein HJ (1978) The effect of weight lifting exercise on heart rate and metabolism in experienced weight lifters. Med Sci Sports 10:13–15

    PubMed  CAS  Google Scholar 

  • Koopman R, Schaart G, Hesselink MK (2001) Optimisation of oil red O staining permits combination with immunofluorescence and automated quantification of lipids. Histochem Cell Biol 116:63–68

    PubMed  CAS  Google Scholar 

  • Koopman R, Manders RJ, Zorenc AH, Hul GB, Kuipers H, Keizer HA, van Loon LJ (2005) A single session of resistance exercise enhances insulin sensitivity for atleast 24 h in healthy men. Eur J Appl Physiol 94:180–187

    Article  PubMed  CAS  Google Scholar 

  • Kraemer WJ, Fry AC (1995) Strength testing: development and evaluation of methodology. In: Maud PJ, Leeds FC (eds) Physiological assessment of human fitness. Human kinetics, UK, pp 115–133

    Google Scholar 

  • Mabuchi K, Sreter FA (1980) Actomyosin ATPase. II. Fiber typing by histochemical ATPase reaction. Muscle Nerve 3:233–239

    Article  PubMed  CAS  Google Scholar 

  • Macaluso A, De Vito G (2004) Muscle strength, power and adaptations to resistance training in older people. Eur J Appl Physiol 91:450–472

    Article  PubMed  Google Scholar 

  • Mayhew JL, Prinster JL, Ware JS, Zimmer DL, Arabas JR, Bemben MG (1995) Muscular endurance repetitions to predict bench press strength in men of different training levels. J Sports Med Phys Fitness 35:108–113

    PubMed  CAS  Google Scholar 

  • Mikines KJ, Sonne B, Farrell PA, Tronier B, Galbo H (1988) Effect of physical exercise on sensitivity and responsiveness to insulin in humans. Am J Physiol 254:E248–E259

    PubMed  CAS  Google Scholar 

  • Miller WJ, Sherman WM, Ivy JL (1984) Effect of strength training on glucose tolerance and post-glucose insulin response. Med Sci Sports Exerc 16:539–543

    PubMed  CAS  Google Scholar 

  • Nielsen JN, Richter EA (2003) Regulation of glycogen synthase in skeletal muscle during exercise. Acta Physiol Scand 178:309–319

    Article  PubMed  CAS  Google Scholar 

  • Oakes ND, Bell KS, Furler SM, Camilleri S, Saha AK, Ruderman NB, Chisholm DJ, Kraegen EW (1997a) Diet-induced muscle insulin resistance in rats is ameliorated by acute dietary lipid withdrawal or a single bout of exercise: parallel relationship between insulin stimulation of glucose uptake and suppression of long-chain fatty acyl-CoA. Diabetes 46:2022–2028

    Article  CAS  Google Scholar 

  • Oakes ND, Camilleri S, Furler SM, Chisholm DJ, Kraegen EW (1997b) The insulin sensitizer, BRL 49653, reduces systemic fatty acid supply and utilization and tissue lipid availability in the rat. Metabolism 46:935–942

    Article  CAS  Google Scholar 

  • Perseghin G, Price TB, Petersen KF, Roden M, Cline GW, Gerow K, Rothman DL, Shulman GI (1996) Increased glucose transport-phosphorylation and muscle glycogen synthesis after exercise training in insulin-resistant subjects. N Engl J Med 335:1357–1362

    Article  PubMed  CAS  Google Scholar 

  • Pruchnic R, Katsiaras A, He J, Kelley DE, Winters C, Goodpaster BH (2004) Exercise training increases intramyocellular lipid and oxidative capacity in older adults. Am J Physiol Endocrinol Metab 287:E857–E862

    Article  PubMed  CAS  Google Scholar 

  • Schaart G, Hesselink RP, Keizer HA, Van Kranenburg G, Drost MR, Hesselink MK (2004) A modified PAS stain combined with immunofluorescence for quantitative analyses of glycogen in muscle sections. Histochem Cell Biol 122:161–169

    Article  PubMed  CAS  Google Scholar 

  • Schrauwen-Hinderling VB, van Loon LJ, Koopman R, Nicolay K, Saris WH, Kooi ME (2003) Intramyocellular lipid content is increased after exercise in nonexercising human skeletal muscle. J Appl Physiol 95:2328–2332

    PubMed  CAS  Google Scholar 

  • Siri WE (1956) The gross composition of the body. Adv Biol Med Physiol 4:238–280

    Google Scholar 

  • Stannard SR, Thompson MW, Fairbairn K, Huard B, Sachinwalla T, Thompson CH (2002) Fasting for 72 h increases intramyocellular lipid content in nondiabetic, physically fit men. Am J Physiol Endocrinol Metab 283:E1185–E1191

    PubMed  CAS  Google Scholar 

  • Tesch PA, Colliander EB, Kaiser P (1986) Muscle metabolism during intense, heavy-resistance exercise. Eur J Appl Physiol Occup Physiol 55:362–366

    Article  PubMed  CAS  Google Scholar 

  • Tsintzas K, Williams C, Constantin-Teodosiu D, Hultman E, Boobis L, Greenhaff P (2000) Carbohydrate ingestion prior to exercise augments the exercise-induced activation of the pyruvate dehydrogenase complex in human skeletal muscle. Exp Physiol 85:581–586

    Article  PubMed  CAS  Google Scholar 

  • van Loon LJ, Koopman R, Stegen JH, Wagenmakers AJ, Keizer HA, Saris WH (2003a) Intramyocellular lipids form an important substrate source during moderate intensity exercise in endurance-trained males in a fasted state. J Physiol 553:611–625

    Article  CAS  Google Scholar 

  • van Loon LJ, Schrauwen-Hinderling VB, Koopman R, Wagenmakers AJ, Hesselink MK, Schaart G, Kooi ME, Saris WH (2003b) Influence of prolonged endurance cycling and recovery diet on intramuscular triglyceride content in trained males. Am J Physiol Endocrinol Metab 285:E804–E811

    Google Scholar 

  • van Loon LJ, Koopman R, Manders R, van der Weegen W, van Kranenburg GP, Keizer HA (2004) Intramyocellular lipid content in type 2 diabetes patients compared with overweight sedentary men and highly trained endurance athletes. Am J Physiol Endocrinol Metab 287:E558–565

    Article  PubMed  Google Scholar 

  • van Loon LJ and Goodpaster BH (2005) Increased intramuscular lipid storage in the insulin-resistant and endurance-trained state. Pflugers Arch

  • Watt MJ, Heigenhauser GJ, Spriet LL (2002) Intramuscular triacylglycerol utilization in human skeletal muscle during exercise: is there a controversy? J Appl Physiol 93:1185–1195

    PubMed  CAS  Google Scholar 

  • Wojtaszewski JF, Hansen BF, Kiens B, Richter EA (1997) Insulin signaling in human skeletal muscle: time course and effect of exercise. Diabetes 46:1775–1781

    PubMed  Article  CAS  Google Scholar 

  • Wojtaszewski JF, Hansen BF, Gade, Kiens B, Markuns JF, Goodyear LJ, Richter EA (2000) Insulin signaling and insulin sensitivity after exercise in human skeletal muscle. Diabetes 49:325–331

    PubMed  Article  CAS  Google Scholar 

  • Wojtaszewski JF, Jorgensen SB, Frosig C, MacDonald C, Birk JB, Richter EA (2003) Insulin signalling: effects of prior exercise. Acta Physiol Scand 178:321–328

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to René Koopman.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Koopman, R., Manders, R.J.F., Jonkers, R.A.M. et al. Intramyocellular lipid and glycogen content are reduced following resistance exercise in untrained healthy males. Eur J Appl Physiol 96, 525–534 (2006). https://doi.org/10.1007/s00421-005-0118-0

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00421-005-0118-0

Keywords

  • Carbohydrate
  • IMTG
  • Skeletal muscle
  • Metabolism
  • Oxidative capacity