Skip to main content
Log in

Skeletal muscle ATP turnover and single fibre ATP and PCr content during intense exercise at different muscle temperatures in humans

  • Muscle Physiology
  • Published:
Pflügers Archiv - European Journal of Physiology Aims and scope Submit manuscript

Abstract

The effect of temperature on skeletal muscle ATP turnover, pulmonary oxygen uptake and single fibre ATP and PCr content was studied during intense cycling exercise. Six healthy male subjects performed 6-min intense (Δ50%LT-VO2peak) cycling, at 60 rpm, under conditions of normal (N) and elevated muscle temperature (ET). Muscle biopsies obtained from the vastus lateralis at rest, 2 and 6 min were analysed for homogenate ATP, PCr, lactate and glycogen, allowing estimation of anaerobic ATP turnover. Freeze-dried single fibres from biopsies were characterised according to their myosin heavy chain composition (type I, IIA or IIAX) and analysed for ATP and PCr content. Pulmonary gas exchange was measured throughout. There was no difference in pulmonary oxygen uptake between the trials. The elevation of muscle temperature resulted in a lower (P < 0.05) PCr content, higher (P < 0.05) lactate content and greater (P < 0.05) anaerobic ATP turnover after 2 min of exercise. There was no effect of temperature on these measures at 6 min. In single fibres it was observed that in ET, there was a lower (P < 0.05) PCr content in type I fibres after 2 min with no differences between conditions after 6 min. The present study demonstrates that elevation of muscle temperature results in a greater anaerobic ATP turnover and type I fibre PCr degradation during the initial 2 min of intense exercise.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Asmussen E, Boje O (1945) Body temperature and the capacity for work. Acta Physiol Scand 10:1–22

    Article  Google Scholar 

  2. Bangsbo J, Gollink PD, Graham TE, Juel C, Kiens B, Mizuno M, Saltin B (1990) Anaerobic energy production and O2 deficit–debt relationship during exhaustive exercise in humans. J Physiol 422:539–559

    PubMed  CAS  Google Scholar 

  3. Beaver WL, Wasserman K, Whipp BJ (1985) Improved detection of lactate threshold during exercise using a log–log transformation. J Appl Physiol 59:1936–1940

    PubMed  CAS  Google Scholar 

  4. Bell MP, Ferguson RA (2009) Interaction between muscle temperature and contraction velocity affects mechanical efficiency during moderate-intensity cycling exercise in young and older women. Journal of Applied Physiology 107:763–769

    Article  PubMed  Google Scholar 

  5. Beltman JG, de Haan A, Haan H, Gerrits HL, van Mechelen W, Sargeant AJ (2004) Metabolically assessed muscle fibre recruitment in brief isometric contractions at different intensities. Eur J Appl Physiol 92:485–492

    Article  PubMed  CAS  Google Scholar 

  6. Beltman JG, Sargeant AJ, Haan H, van Mechelen W, de Haan A (2004) Changes in PCr/Cr ratio on single characterized muscle fibre fragments after only a few maximal voluntary contractions in humans. Acta Physiol Scand 180:187–193

    Article  PubMed  CAS  Google Scholar 

  7. Bennett AF (1984) Thermal dependence of muscle function. Am J Physiol 247:R217–R229

    PubMed  CAS  Google Scholar 

  8. Bergstrom J (1962) Muscle electrolytes in man. Scand J Clin Lab Invest suppl 68:1–101

    Google Scholar 

  9. Burnley M, Doust JH, Ball D, Jones AM (2002) Effects of prior heavy exercise on Vo2 kinetics during heavy exercise are related to changes in muscle activity. J Appl Physiol 93:167–174

    PubMed  Google Scholar 

  10. Burnley M, Doust JH, Jones AM (2002) Effects of prior heavy exercise, prior sprint exercise and passive warming on oxygen uptake kinetics during heavy exercise in humans. Eur J Appl Physiol 87:424–432

    Article  PubMed  CAS  Google Scholar 

  11. Conjard A, Pette D (1999) Phosphocreatine as a marker of contractile activity in single muscle fibres. Pflugers Archiv 438:278–282

    Article  PubMed  CAS  Google Scholar 

  12. di Prampero PE, Ferretti G (1999) The energetics of anaerobic muscle metabolism: a reappraisal of older and recent concepts. Respiration Physiology 118:103–115

    Article  PubMed  Google Scholar 

  13. Edwards RHT, Harris RC, Hultman E, Kaijser L, Koh D, Nordesjo L-O (1972) Effect of temperature on muscle energy metabolism and endurance during successive isometric contractions, sustained to fatigue, of the quadriceps muscle in man. J Physiol 220:335–352

    PubMed  CAS  Google Scholar 

  14. Fauteck SP, Kandarian SC (1995) Sensitive detection of myosin heavy chain composition in skeletal muscle under different loading conditions. Am J Physiol 268:C419–C424

    PubMed  CAS  Google Scholar 

  15. Febbraio MA (2000) Does muscle function and metabolism affect exercise performance in the heat? Exerc Sport Sci Rev 28:171–176

    PubMed  CAS  Google Scholar 

  16. Febbraio MA, Carey MF, Snow RJ, Stathis CG, Hargreaves M (1996) Influence of elevated muscle temperature on metabolism during intense, dynamic exercise. Am J Physiol 271:1251–1255

    Google Scholar 

  17. Fenn WO (1923) A quantitative comparison between the energy liberated and the work performed by the isolated sartorius muscle of the frog. J Physiol 58:175–203

    PubMed  CAS  Google Scholar 

  18. Ferguson RA, Ball D, Sargeant AJ (2002) Effect of muscle temperature on rate of oxygen uptake during exercise in humans at different contraction frequencies. J Exp Biol 205:981–987

    PubMed  Google Scholar 

  19. Ferguson RA, Krustrup P, Kjaer M, Mohr M, Ball D, Bangsbo J (2006) Effect of temperature on skeletal muscle energy turnover during dynamic knee-extensor exercise in humans. J Appl Physiol 101:47–52

    Article  PubMed  CAS  Google Scholar 

  20. Gladden LB (2000) Muscle as a consumer of lactate. Med Sci Sports Exerc 32:764–771

    Article  PubMed  CAS  Google Scholar 

  21. Gladden LB (2004) Lactate metabolism: a new paradigm for the third millennium. J Physiol 558:5–30

    Article  PubMed  CAS  Google Scholar 

  22. Gollnick PD, Armstrong RB, Saubert CW, Piehl K, Saltin B (1972) Enzyme activity and fiber composition in skeletal muscle of untrained and trained men. Journal of Applied Physiology 33:312–319

    PubMed  CAS  Google Scholar 

  23. Gray SR, De Vito G, Nimmo MA, Farina D, Ferguson RA (2006) Skeletal muscle ATP turnover and muscle fiber conduction velocity are elevated at higher muscle temperatures during maximal power output development in humans. Am J Physiol 290:R376–R382

    Article  CAS  Google Scholar 

  24. Gray SR, Soderlund K, Ferguson RA (2008) ATP and phosphocreatine utilization in single human muscle fibres during the development of maximal power output at elevated muscle temperatures. J Sports Sci 26:701–707

    Article  PubMed  Google Scholar 

  25. Greenhaff PL, Nevill AM, Söderlund K, Bodin K, Boobis LH, Williams C, Hultman E (1994) The metabolic responses of human type I and II muscle fibres during maximal treadmill sprinting. J Physiol 478:149–155

    PubMed  Google Scholar 

  26. Harris RC, Hultman E, Nordesjö L-O (1974) Glycogen, glycolytic intermediates and high-energy phosphates determined in biopsy samples of musculus quadriceps femoris of man at rest. Methods and variance of values. Scand J Clin Lab Invest 33:109–120

    Article  PubMed  CAS  Google Scholar 

  27. He Z-H, Bottinelli R, Pellegrino MA, Ferenczi MA, Reggiani C (2000) ATP consumption and efficiency of human single muscle fibres with different myosin isoform composition. Biophysical Journal 79:945–961

    Article  PubMed  CAS  Google Scholar 

  28. Infante AA, Klaupiks D, Davies RE (1965) Phosphorylcreatine consumption during single-working contractions of isolated muscle. Biochim Biophys Acta 94:504–515

    Article  PubMed  CAS  Google Scholar 

  29. Jones. AM (1998) A five year physiological case study of an olympic runner. Br J Sp Med 32:39–43

    Google Scholar 

  30. Karatzaferi C, Chinn MK, Cooke R (2004) The force exerted by a muscle cross-bridge depends directly on the strength of the actomyosin bond. Biophysical Journal 87:2532–2544

    Article  PubMed  CAS  Google Scholar 

  31. Koga S, Shiojiri T, Kondo N, Barstow TJ (1997) Effect of increased muscle temperature on oxygen uptake kinetics during exercise. J Appl Physiol 83:1333–1338

    PubMed  CAS  Google Scholar 

  32. Larsson L, Moss RL (1993) Maximum velocity of shortening in relation to myosin isoform composition in single fibres from human skeletal muscles. J Physiol 472:595–614

    PubMed  CAS  Google Scholar 

  33. Lowry OH, Passonneau JV (1972) A flexible system of enzymatic analysis. Academic, New York

    Google Scholar 

  34. Medbo JI, Tabata I (1993) Anaerobic energy release in working muscle during 30s to 3 min of exhausting bicycling. J Appl Physiol 75:1654–1660

    PubMed  CAS  Google Scholar 

  35. Oakley BR, Kirsch DR, Morris NR (1980) A simplified ultrasensitive silver stain for detecting proteins in polyacrylamide gels. Analytical Biochemistry 105(1):361–363

    Google Scholar 

  36. Parolin ML, Chesley A, Matsos MP, Spriet LL, Jones NL, Heigenhauser GJF (1999) Regulation of skeletal muscle glycogen phoshorylase and PDH during maximal intermittent exercise. Am J Physiol 277:E890–E900

    PubMed  CAS  Google Scholar 

  37. Rall JA, Woledge RC (1990) Influence of temperature on mechanics and energetics of muscle contraction. Am J Physiol 259:197–203

    Google Scholar 

  38. Ranatunga KW (1984) The force–velocity relation of rat fast- and slow-twitch muscles examined at different temperatures. J Physiol 351:517–529

    PubMed  CAS  Google Scholar 

  39. Saltin B, Gagge AP, Stolwijk JAJ (1968) Muscle temperature during submaximal exercise in man. J Appl Physiol 25:679–688

    PubMed  CAS  Google Scholar 

  40. Sargeant AJ, Jones DA (1995) The significance of motor unit variability in sustaining mechanical output of muscle. In: Gandevia SC, Enoka RM, McComas AJ, Stuart DG, Thomas CK (eds) Fatigue: neural and muscular mechanisms. Plenum, New York, pp 323–338

    Google Scholar 

  41. Sargeant AJ, Rademaker A (1996) Human muscle power in the locomotory range of contraction velocities increases with temperature due to an increase in power generated by type I fibres. J Physiol 491:128P

    Google Scholar 

  42. Spriet LL (1995) Anaerobic metabolism during high-intensity exercise. In: Hargreaves M (ed) Exercise metabolism. Human Kinetics, Illinois, pp 1–40

    Google Scholar 

  43. Spriet LL, Söderlund K, Bergstrom M, Hultman E (1987) Anaerobic energy release in skeletal muscle during electrical stimulation in men. J Appl Physiol 62:611–615

    Article  PubMed  CAS  Google Scholar 

  44. Starkie RL, Hargreaves M, Lambert DL, Proietto J, Febbraio MA (1999) Effect of temperature on muscle metabolism during submaximal exercise in humans. Exp Physiol 84:775–784

    Article  PubMed  CAS  Google Scholar 

  45. Steinen GJM, Kiers JL, Bottinelli R, Reggiani C (1996) Myofibrillar ATPase activity in skinned human skeletal muscle fibres: fibre types and temperature dependence. J Physiol 493:299–307

    Google Scholar 

  46. Wibom R, Söderlund K, Lundin A, Hultman E (1991) A luminometric method for the determination of ATP and phosphocreatine in single human skeletal muscle fibres. J Biolumin and Chemilumin 6:123–129

    Article  CAS  Google Scholar 

  47. Wyss M, Schlegel J, James P, Eppenberger HM, Wallimann T (1990) Mitochondrial creatine kinase from chicken brain. Purification, biophysical characterization, and generation of heterodimeric and heterooctameric molecules with subunits of other creatine kinase isoenzymes. J Biol Chem 265:15900–15908

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Stuart R. Gray.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gray, S.R., Soderlund, K., Watson, M. et al. Skeletal muscle ATP turnover and single fibre ATP and PCr content during intense exercise at different muscle temperatures in humans. Pflugers Arch - Eur J Physiol 462, 885–893 (2011). https://doi.org/10.1007/s00424-011-1032-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00424-011-1032-4

Keywords

Navigation