Does oxidative capacity affect energy cost? An in vivo MR investigation of skeletal muscle energetics

European Journal of Applied Physiology

Volumn 106, Issue 2, 2009, Pages 229-242

  Layec, Gwenael ^a   Bringard, Aurélien ^b   Vilmen, Christophe ^a   Micallef, Jean Paul ^b,c   Le Fur, Yann ^a   Perrey, Stéphane ^b   Cozzone, Patrick J ^a   Bendahan, David ^a  

^a CNRS   (France)

^b UNIV MONTPELLIER   (France)

^c INSERM   (France)

Author keywords

ATP production; Endurance training; Exercise efficiency; Magnetic resonance spectroscopy; Muscle metabolism; Oxygen uptake

Indexed keywords

ADENOSINE TRIPHOSPHATE;

ADULT; AEROBIC CAPACITY; ANAEROBIC CAPACITY; ARTICLE; CONTROLLED STUDY; ENDURANCE; ENERGY COST; EXERCISE INTENSITY; FEMALE; HUMAN; HUMAN EXPERIMENT; IN VIVO STUDY; LEG EXERCISE; MALE; MITOCHONDRIAL RESPIRATION; MUSCLE CONTRACTION; MUSCLE METABOLISM; NORMAL HUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; OXYGEN CONSUMPTION; PHOSPHORUS NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; QUADRICEPS FEMORIS MUSCLE; REST; SITTING; SKELETAL MUSCLE;

ADENOSINE TRIPHOSPHATE; ADULT; ANAEROBIOSIS; HUMANS; MAGNETIC RESONANCE SPECTROSCOPY; MALE; MUSCLE, SKELETAL; OXIDATION-REDUCTION; OXYGEN CONSUMPTION; PHYSICAL ENDURANCE;

EID: 67349145243     PISSN: 14396319     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00421-009-1012-y     Document Type: Article

References (97)

1. Adams GR, Foley JM, Meyer RA (1990) Muscle buffer capacity estimated from pH changes during rest-to-work transitions. J Appl Physiol 69:968-972
2. Allen DG, Lamb GD, Westerblad H (2008) Skeletal muscle fatigue: Cellular mechanisms. Physiol Rev 88:287-332
3. Armstrong RB, Laughlin MH (1984) Exercise blood flow patterns within and among rat muscles after training. Am J Physiol 246:H59-H68
4. Bendahan D, Mattei JP, Ghattas B, Confort-Gouny S, Le Guern ME, Cozzone PJ (2002) Citrulline/malate promotes aerobic energy production in human exercising muscle. Br J Sports Med 36:282-289
5. Boska M (1991) Estimating the ATP cost of force production in the human gastrocnemius/soleus muscle group using 31P MRS and 1H MRI. NMR Biomed 4:173-181
6. Boska M (1994) ATP production rates as a function of force level in the human gastrocnemius/soleus using 31P MRS. Magn Reson Med 32:1-10
7. Brown TR, Stoyanova R, Greenberg T, Srinivasan R, Murphy-Boesch J (1995) NOE enhancements and T1 relaxation times of phosphorylated metabolites in human calf muscle at 1.5 Tesla. Magn Reson Med 33:417-421
8. Burgomaster KA, Cermak NM, Phillips SM, Benton CR, Bonen A, Gibala MJ (2007) Divergent response of metabolite transport proteins in human skeletal muscle after sprint interval training and detraining. Am J Physiol Regul Integr Comp Physiol 292:R1970-R1976
9. Chance B, Williams GR (1955) Respiratory enzymes in oxidative phosphorylation. IV. The respiratory chain. J Biol Chem 217:429-438
10. Chance B, Leigh JS Jr, Kent J, McCully K, Nioka S, Clark BJ, Maris JM, Graham T (1986) Multiple controls of oxidative metabolism in living tissues as studied by phosphorus magnetic resonance. Proc Natl Acad Sci USA 83:9458-9462
11. Clark BJ 3rd, Acker MA, McCully K, Subramanian HV, Hammond RL, Salmons S, Chance B, Stephenson LW (1988) In vivo 31P-NMR spectroscopy of chronically stimulated canine skeletal muscle. Am J Physiol 254:C258-C266
12. Coggan AR, Spina RJ, King DS, Rogers MA, Brown M, Nemeth PM, Holloszy JO (1992) Skeletal muscle adaptations to endurance training in 60- to 70-yr-old men and women. J Appl Physiol 72:1780-1786
13. Conley KE, Blei ML, Richards TL, Kushmerick MJ, Jubrias SA (1997) Activation of glycolysis in human muscle in vivo. Am J Physiol 273:C306-C315
14. Conley KE, Kushmerick MJ, Jubrias SA (1998) Glycolysis is independent of oxygenation state in stimulated human skeletal muscle in vivo. J Physiol 511(Pt 3):935-945
15. Coyle EF (2005) Improved muscular efficiency displayed as Tour de France champion matures. J Appl Physiol 98:2191-2196
16. Coyle EF, Coggan AR, Hopper MK, Walters TJ (1988) Determinants of endurance in well-trained cyclists. J Appl Physiol 64:2622-2630
17. Coyle EF, Feltner ME, Kautz SA, Hamilton MT, Montain SJ, Baylor AM, Abraham LD, Petrek GW (1991) Physiological and biomechanical factors associated with elite endurance cycling performance. Med Sci Sports Exerc 23:93-107
18. Coyle EF, Sidossis LS, Horowitz JF, Beltz JD (1992) Cycling efficiency is related to the percentage of type I muscle fibers. Med Sci Sports Exerc 24:782-788
19. De Luca CJ (1997) The use of surface electromyography in biomechanics. J Appl Biomech 13:135-163
20. Debold EP, Beck SE, Warshaw DM (2008) The effect of low pH on single skeletal muscle myosin mechanics and kinetics. Am J Physiol Cell Physiol 295(1):C173-C179
21. Edge EJ, Bishop D, Hill-Haas S, Dawson B, Goodman C (2006a) Comparison of muscle buffer capacity and repeated-sprint ability of untrained, endurance-trained and team-sport athletes. Eur J Appl Physiol 96:225-234
22. Edge J, Bishop D, Goodman C (2006b) The effects of training intensity on muscle buffer capacity in females. Eur J Appl Physiol 96:97-105
23. Edgerton VR, Smith JL, Simpson DR (1975) Muscle fibre type populations of human leg muscles. Histochem J 7:259-266
24. Fitts RH (2008) The cross-bridge cycle and skeletal muscle fatigue. J Appl Physiol 104:551-558
25. Frontera WR, Meredith CN, O'Reilly KP, Knuttgen HG, Evans WJ (1988) Strength conditioning in older men: Skeletal muscle hypertrophy and improved function. J Appl Physiol 64:1038-1044
26. Gaesser GA, Brooks GA (1975) Muscular efficiency during steady-rate exercise: Effects of speed and work rate. J Appl Physiol 38:1132-1139
27. Gaesser GA, Poole DC (1996) The slow component of oxygen uptake kinetics in humans. Exerc Sport Sci Rev 24:35-71
28. Gissane C, Corrigan DL, White JA (1991) Gross efficiency responses to exercise conditioning in adult males of various ages. J Sports Sci 9:383-391
29. Gollnick PD, Bayly WM, Hodgson DR (1986) Exercise intensity, training, diet, and lactate concentration in muscle and blood. Med Sci Sports Exerc 18:334-340
30. Harris RC, Hultman E, Nordesjo LO (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
31. He ZH, Bottinelli R, Pellegrino MA, Ferenczi MA, Reggiani C (2000) ATP consumption and efficiency of human single muscle fibers with different myosin isoform composition. Biophys J 79:945-961
32. Hermens J, Freriks B, Merletti R, Stegeman D, Blok J, Rau G, Disselhorst-Klug C, Haäg G (1999) European recommendations for surface electromyography. Roessingh Research and Development, The Netherlands
33. Hettinga FJ, De Koning JJ, de Vrijer A, Wust RC, Daanen HA, Foster C (2007) The effect of ambient temperature on gross-efficiency in cycling. Eur J Appl Physiol 101:465-471
34. Hochachka PW, Mommsen TP (1983) Protons and anaerobiosis. Science 219:1391-1397
35. Holloszy JO, Coyle EF (1984) Adaptations of skeletal muscle to endurance exercise and their metabolic consequences. J Appl Physiol 56:831-838
36. 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
37. Horowitz JF, Sidossis LS, Coyle EF (1994) High efficiency of type I muscle fibers improves performance. Int J Sports Med 15:152-157
38. Hug F, Bendahan D, Le Fur Y, Cozzone PJ, Grelot L (2005) Metabolic recovery in professional road cyclists: A 31P-MRS study. Med Sci Sports Exerc 37:846-852
39. Hug F, Grelot L, Le Fur Y, Cozzone PJ, Bendahan D (2006) Recovery kinetics throughout successive bouts of various exercises in elite cyclists. Med Sci Sports Exerc 38:2151-2158
40. Hunter GR, Newcomer BR, Larson-Meyer DE, Bamman MM, Weinsier RL (2001) Muscle metabolic economy is inversely related to exercise intensity and type II myofiber distribution. Muscle Nerve 24:654-661
41. Hunter GR, Bamman MM, Larson-Meyer DE, Joanisse DR, McCarthy JP, Blaudeau TE, Newcomer BR (2005) Inverse relationship between exercise economy and oxidative capacity in muscle. Eur J Appl Physiol 94:558-568
42. Jeneson JA, Wiseman RW, Westerhoff HV, Kushmerick MJ (1996) The signal transduction function for oxidative phosphorylation is at least second order in ADP. J Biol Chem 271:27995-27998
43. Jeukendrup AE, Wallis GA (2005) Measurement of substrate oxidation during exercise by means of gas exchange measurements. Int J Sports Med 26(Suppl 1):S28-S37
44. Johansen L, Quistorff B (2003) 31P-MRS characterization of sprint and endurance trained athletes. Int J Sports Med 24:183-189
45. Jones AM, Carter H (2000) The effect of endurance training on parameters of aerobic fitness. Sports Med 29:373-386
46. Joyner MJ, Coyle EF (2008) Endurance exercise performance: The physiology of champions. J Physiol 586:35-44
47. Jubrias SA, Esselman PC, Price LB, Cress ME, Conley KE (2001) Large energetic adaptations of elderly muscle to resistance and endurance training. J Appl Physiol 90:1663-1670
48. Jubrias SA, Crowther GJ, Shankland EG, Gronka RK, Conley KE (2003) Acidosis inhibits oxidative phosphorylation in contracting human skeletal muscle in vivo. J Physiol 553:589-599
49. Juel C (1998) Muscle pH regulation: Role of training. Acta Physiol Scand 162:359-366
50. Kemp GJ, Radda GK (1994) Quantitative interpretation of bioenergetic data from 31P and 1H magnetic resonance spectroscopic studies of skeletal muscle: An analytical review. Magn Reson Q 10:43-63
51. Kemp GJ, Taylor DJ, Styles P, Radda GK (1993) The production, buffering and efflux of protons in human skeletal muscle during exercise and recovery. NMR Biomed 6:73-83
52. Kemp GJ, Thompson CH, Barnes PR, Radda GK (1994) Comparisons of ATP turnover in human muscle during ischemic and aerobic exercise using 31P magnetic resonance spectroscopy. Magn Reson Med 31:248-258
53. Kemp GJ, Thompson CH, Taylor DJ, Radda GK (1995) ATP production and mechanical work in exercising skeletal muscle: A theoretical analysis applied to 31P magnetic resonance spectroscopic studies of dialyzed uremic patients. Magn Reson Med 33:601-609
54. Kemp GJ, Roussel M, Bendahan D, Le Fur Y, Cozzone PJ (2001) Interrelations of ATP synthesis and proton handling in ischaemically exercising human forearm muscle studied by 31P magnetic resonance spectroscopy. J Physiol 535:901-928
55. Kemper WF, Lindstedt SL, Hartzler LK, Hicks JW, Conley KE (2001) Shaking up glycolysis: Sustained, high lactate flux during aerobic rattling. Proc Natl Acad Sci USA 98:723-728
56. Kent-Braun JA, McCully KK, Chance B (1990) Metabolic effects of training in humans: A 31P-MRS study. J Appl Physiol 69:1165-1170
57. Knuth ST, Dave H, Peters JR, Fitts RH (2006) Low cell pH depresses peak power in rat skeletal muscle fibres at both 30 degrees C and 15 degrees C: Implications for muscle fatigue. J Physiol 575:887-899
58. Kushmerick MJ (1997) Multiple equilibria of cations with metabolites in muscle bioenergetics. Am J Physiol 272:C1739-C1747
59. Lanza IR, Wigmore DM, Befroy DE, Kent-Braun JA (2006) In vivo ATP production during free-flow and ischaemic muscle contractions in humans. J Physiol 577:353-367
60. Laurent D, Reutenauer H, Payen JF, Favre-Juvin A, Eterradossi J, Lebas JF, Rossi A (1992) Muscle bioenergetics in skiers: Studies using NMR spectroscopy. Int J Sports Med 13(Suppl 1):S150-S152
61. Layec G, Bringard A, Vilmen C, Micallef JP, Fur YL, Perrey S, Cozzone PJ, Bendahan D (2008) Accurate work-rate measurements during in vivo MRS studies of exercising human quadriceps. Magma
62. Lucia A, Hoyos J, Perez M, Santalla A, Chicharro JL (2002a) Inverse relationship between VO2max and economy/efficiency in world-class cyclists. Med Sci Sports Exerc 34:2079-2084
63. Lucia A, Hoyos J, Santalla A, Perez M, Chicharro JL (2002b) Kinetics of VO(2) in professional cyclists. Med Sci Sports Exerc 34:320-325
64. Lundby C, Calbet JA, Sander M, van Hall G, Mazzeo RS, Stray-Gundersen J, Stager JM, Chapman RF, Saltin B, Levine BD (2007) Exercise economy does not change after acclimatization to moderate to very high altitude. Scand J Med Sci Sports 17:281-291
65. Mallory LA, Scheuermann BW, Hoelting BD, Weiss ML, McAllister RM, Barstow TJ (2002) Influence of peak VO2 and muscle fiber type on the efficiency of moderate exercise. Med Sci Sports Exerc 34:1279-1287
66. Marsh AP, Martin PE, Foley KO (2000) Effect of cadence, cycling experience, and aerobic power on delta efficiency during cycling. Med Sci Sports Exerc 32:1630-1634
67. Matheson GO, Allen PS, Ellinger DC, Hanstock CC, Gheorghiu D, McKenzie DC, Stanley C, Parkhouse WS, Hochachka PW (1991) Skeletal muscle metabolism and work capacity: A 31P-NMR study of Andean natives and lowlanders. J Appl Physiol 70:1963-1976
68. McKenna MJ, Harmer AR, Fraser SF, Li JL (1996) Effects of training on potassium, calcium and hydrogen ion regulation in skeletal muscle and blood during exercise. Acta Physiol Scand 156:335-346
69. Minotti JR, Johnson EC, Hudson TL, Zuroske G, Fukushima E, Murata G, Wise LE, Chick TW, Icenogle MV (1990) Training-induced skeletal muscle adaptations are independent of systemic adaptations. J Appl Physiol 68:289-294
70. Mogensen M, Bagger M, Pedersen PK, Fernstrom M, Sahlin K (2006) Cycling efficiency in humans is related to low UCP3 content and to type I fibres but not to mitochondrial efficiency. J Physiol 571:669-681
71. Moon RB, Richards JH (1973) Determination of intracellular pH by 31P magnetic resonance. J Biol Chem 248:7276-7278
72. Moseley L, Jeukendrup AE (2001) The reliability of cycling efficiency. Med Sci Sports Exerc 33:621-627
73. Moseley L, Achten J, Martin JC, Jeukendrup AE (2004) No differences in cycling efficiency between world-class and recreational cyclists. Int J Sports Med 25:374-379
74. Newcomer BR, Boska MD (1999) T1 measurements of 31P metabolites in resting and exercising human gastrocnemius/soleus muscle at 1.5 Tesla. Magn Reson Med 41:486-494
75. Pilegaard H, Bangsbo J, Richter EA, Juel C (1994) Lactate transport studied in sarcolemmal giant vesicles from human muscle biopsies: relation to training status. J Appl Physiol 77:1858-1862
76. Pilegaard H, Bangsbo J, Henningsen P, Juel C, Richter EA (1995) Effect of blood flow on muscle lactate release studied in perfused rat hindlimb. Am J Physiol 269:E1044-E1051
77. Poole DC, Schaffartzik W, Knight DR, Derion T, Kennedy B, Guy HJ, Prediletto R, Wagner PD (1991) Contribution of excising legs to the slow component of oxygen uptake kinetics in humans. J Appl Physiol 71:1245-1260
78. Quistorff B, Johansen L, Sahlin K (1993) Absence of phosphocreatine resynthesis in human calf muscle during ischaemic recovery. Biochem J 291(Pt 3):681-686
79. Reggiani C, Potma EJ, Bottinelli R, Canepari M, Pellegrino MA, Stienen GJ (1997) Chemo-mechanical energy transduction in relation to myosin isoform composition in skeletal muscle fibres of the rat. J Physiol 502(Pt 2):449-460
80. Rossiter HB, Ward SA, Howe FA, Kowalchuk JM, Griffiths JR, Whipp BJ (2002) Dynamics of intramuscular 31P-MRS P(i) peak splitting and the slow components of PCr and O2 uptake during exercise. J Appl Physiol 93:2059-2069
81. Roussel M, Bendahan D, Mattei JP, Le Fur Y, Cozzone PJ (2000) 31P magnetic resonance spectroscopy study of phosphocreatine recovery kinetics in skeletal muscle: The issue of intersubject variability. Biochim Biophys Acta 1457:18-26
82. Ryschon TW, Fowler MD, Wysong RE, Anthony A, Balaban RS (1997) Efficiency of human skeletal muscle in vivo: Comparison of isometric, concentric, and eccentric muscle action. J Appl Physiol 83:867-874
83. Sahlin K (2005) Determination of muscle pH and glycolytic flux by magnetic resonance spectroscopy in contracting human skeletal muscle may have systematic errors. Am J Physiol Cell Physiol 289:C230; author reply C231
84. Saltin B (1985) Hemodynamic adaptations to exercise. Am J Cardiol 55:42D-47D
85. Scheuermann BW, Hoelting BD, Noble ML, Barstow TJ (2001) The slow component of O(2) uptake is not accompanied by changes in muscle EMG during repeated bouts of heavy exercise in humans. J Physiol 531:245-256
86. Sharp RL, Costill DL, Fink WJ, King DS (1986) Effects of eight weeks of bicycle ergometer sprint training on human muscle buffer capacity. Int J Sports Med 7:13-17
87. Sharwood KA, Lambert MI, St Clair Gibson A, Noakes TD (2000) Changes in muscle power and neuromuscular efficiency after a 40-minute downhill run in veteran long distance runners. Clin J Sport Med 10:129-135
88. Stubbs M, Van den Boogaart A, Bashford CL, Miranda PM, Rodrigues LM, Howe FA, Griffiths JR (1996) 31P-magnetic resonance spectroscopy studies of nucleated and non-nucleated erythrocytes; time domain data analysis (VARPRO) incorporating prior knowledge can give information on the binding of ADP. Biochim Biophys Acta 1291:143-148
89. Trenell MI, Sue CM, Kemp GJ, Sachinwalla T, Thompson CH (2006) Aerobic exercise and muscle metabolism in patients with mitochondrial myopathy. Muscle Nerve 33:524-531
90. van den Broek NM, De Feyter HM, de Graaf L, Nicolay K, Prompers JJ (2007) Intersubject differences in the effect of acidosis on phosphocreatine recovery kinetics in muscle after exercise are due to differences in proton efflux rates. Am J Physiol Cell Physiol 293:C228-C237
91. van der Veen JW, de Beer R, Luyten PR, van Ormondt D (1988) Accurate quantification of in vivo 31P NMR signals using the variable projection method and prior knowledge. Magn Reson Med 6:92-98
92. Vandenborne K, Walter G, Ploutz-Snyder L, Staron R, Fry A, De Meirleir K, Dudley GA, Leigh JS (1995) Energy-rich phosphates in slow and fast human skeletal muscle. Am J Physiol 268:C869-C876
93. Vanhamme L, van den Boogaart A, Van Huffel S (1997) Improved method for accurate and efficient quantification of MRS data with use of prior knowledge. J Magn Reson 129:35-43
94. Walter G, Vandenborne K, Elliott M, Leigh JS (1999) In vivo ATP synthesis rates in single human muscles during high intensity exercise. J Physiol 519(Pt 3):901-910
95. Wigmore DM, Damon BM, Pober DM, Kent-Braun JA (2004) MRI measures of perfusion-related changes in human skeletal muscle during progressive contractions. J Appl Physiol 97:2385-2394
96. Wilkerson DP, Koppo K, Barstow TJ, Jones AM (2004) Effect of work rate on the functional 'gain' of Phase II pulmonary O2 uptake response to exercise. Respir Physiol Neurobiol 142:211-223
97. Zoll J, Sanchez H, N'Guessan B, Ribera F, Lampert E, Bigard X, Serrurier B, Fortin D, Geny B, Veksler V, Ventura-Clapier R, Mettauer B (2002) Physical activity changes the regulation of mitochondrial respiration in human skeletal muscle. J Physiol 543:191-200