Ex vivo measures of muscle mitochondrial capacity reveal quantitative limits of oxygen delivery by the circulation during exercise

International Journal of Biochemistry and Cell Biology

Volumn 45, Issue 1, 2013, Pages 68-75

  Boushel, Robert ^a   Saltin, Bengt ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

Exercise; Oxidative phosphorylation

Indexed keywords

OXYGEN;

BODY MASS; EX VIVO STUDY; EXERCISE; HUMAN; IN VIVO STUDY; METABOLIC CAPACITY; MUSCLE BLOOD FLOW; MUSCLE MASS; MUSCLE MITOCHONDRIAL RESPIRATORY CAPACITY; OXYGEN CONSUMPTION; REVIEW;

EID: 84870724597     PISSN: 13572725     EISSN: 18785875     Source Type: Journal    
DOI: 10.1016/j.biocel.2012.09.024     Document Type: Article

References (88)

1. G. Ahlborg, and M. Jensen-Urstad Arm blood flow at rest and during arm exercise Journal of Applied Physiology 70 1991 928 933
2. W. Ament, J. Lubbers, G. Rakhorst, W. Vaalburg, G.J. Verkerke, and A.M. Paans Skeletal muscle perfusion measured by positron emission tomography during exercise Pflugers Archiv: European Journal of Physiology 436 5 1998 653 658
3. P. Andersen, and B. Saltin Maximal perfusion of skeletal muscle in man The Journal of Physiology 366 1985 233 249
4. F. Appaix, A.V. Kuznetsov, Y. Usson, L. Kay, T. Andrienko, and J. Olivares Possible role of cytoskeleton in intracellular arrangement and regulation of mitochondria Experimental Physiology 88 1 2003 175 190
5. D. Bach, S. Pich, F.X. Soriano, N. Vega, B. Baumgartner, and J. Oriola Mitofusin-2 determines mitochondrial network architecture and mitochondrial metabolism: a novel regulatory mechanism altered in obesity Journal of Biological Chemistry 278 19 2003 17190 17197
6. G. Benard, and R. Rossignol Ultrastructure of the mitochondrion and its bearing on function and bioenergetics Antioxidants and Redox Signalling 10 8 2008 1313 1342
7. B.R. Berg, and I.H. Sarelius Functional capillary organization in striated muscle American Journal of Physiology 268 3 Pt 2 1995 H1215 H1222
8. E. Blomstrand, G. Radegran, and B. Saltin Maximum rate of oxygen uptake by human skeletal muscle in relation to maximal activities of enzymes in the Krebs cycle The Journal of Physiology 501 2 1997 455 460
9. E. Blomstrand, P. Krustrup, H. Sondergaard, G. Radegran, J.A. Calbet, and B. Saltin Exercise training induces similar elevations in the activity of oxoglutarate dehydrogenase and peak oxygen uptake in the human quadriceps muscle Pflugers Archiv: European Journal of Physiology 462 2 2011 257 265
10. R. Boushel, E. Gnaiger, P. Schjerling, M. Skovbro, R. Kraunsoe, and F. Dela Patients with type 2 diabetes have normal mitochondrial function in muscle Diabetologia 50 2007 790 796
11. Boushel, E. Gnaiger, C. Wright-Paradis, J.A. Calbet, J. González-Alonso, and T. Munch-Andersen Muscle mitochondrial capacity exceeds maximal oxygen delivery in humans Mitochondrion 11 2 2011 303 307
12. J.A. Calbet, R. Boushel, G. Radegran, H. Sondergaard, P.D. Wagner, and B. Saltin Determinants of maximal oxygen uptake in severe acute hypoxia American Journal of Physiology: Regulatory, Integrative and Comparative Physiology 284 2 2003 R291 R303
13. J.A. Calbet, M. Jensen-Urstad, G. Van Hall, H.C. Holmberg, H. Rosdahl, and B. Saltin Maximal muscular vascular conductances during whole body upright exercise in humans The Journal of Physiology 558 Pt 1 2004 319 331
14. J.A. Calbet, H.C. Holmberg, H. Rosdahl, G. van Hall, M. Jensen-Urstad, and B. Saltin Why do arms extract less oxygen than legs during exercise? American Journal of Physiology: Regulatory, Integrative and Comparative Physiology 289 5 2005 R1448 R1458
15. 2 extraction during maximal exercise in humans American Journal of Physiology: Regulatory, Integrative and Comparative Physiology 291 2 2006 R447 R453
16. J.A. Calbet, J. Gonzalez-Alonso, J.W. Helge, H. Sondergaard, T. Munich-Andersen, and R. Boushel Cardiac output, and leg and arm blood flow during incremental exercise to exhaustion on the cycle ergometer Journal of Applied Physiology 103 3 2007 969 978
17. B. Chance, and G.R. Williams Respiratory enzymes in oxidative phosphorylation VI. The effects of adenosine diphosphate on azide-treated mitochondria Journal of Biological Chemistry 221 1 1956 477 489
18. H. Chen, and D.C. Chan Physiological functions of mitochondrial fusion Proceedings of the National Academy of Sciences of the United States of America 1201 2010 21 25
19. G.J. Cooney, H. Taegtmeyer, and E.A. Newsholme Tricarboxylic acid cycle flux and enzyme activities in the isolated working rat heart The Biochemical Journal 200 1981 701 703
20. J.M. Dawson, K.R. Tyler, and O. Hudlicka A comparison of the microcirculation in rat fast glycolytic and slow oxidative muscles at rest and during contractions Microvascular Research 33 2 1987 167 182
21. J.A. Dempsey, L. Romer, J. Rodman, J. Miller, and C. Smith Consequences of exercise-induced respiratory muscle work Respiratory Physiology & Neurobiology 151 2-3 2006 242 250
22. L.R. Frank, E.C. Wong, L.J. Haseler, and R.B. Buxton Dynamic imaging of perfusion in human skeletal muscle during exercise with arterial spin labeling Magnetic Resonance in Medicine 42 2 1999 258 267
23. E. Gnaiger Capacity of oxidative phosphorylation in human skeletal muscle: new perspectives of mitochondrial physiology The International Journal of Biochemistry & Cell Biology 41 10 2009 1837 1845
24. E. Gnaiger, B. Lassnig, A. Kuznetsov, G. Reiger, and R. Margreiter Mitochondrial oxygen affinity, respiratory flux control and excess capacity of cytochrome c oxidase Journal of Experimental Biology 201 Pt 8 1998 1129 1139
25. P.D. Gollnick, L.A. Bertocci, T.S. Kelso, E.H. Witt, and D.R. Hodgson The effect of high intensity training on the respiratory capacity of skeletal muscle Pflugers Archiv: European Journal of Physiology 415 1990 407 413
26. J. Gonzalez-Alonso, and J.A. Calbet Reductions in systemic and skeletal muscle blood flow and oxygen delivery limit maximal aerobic capacity in humans Circulation 107 6 2003 824 830
27. D. Hargreaves, S. Egginton, and O. Hudlicka Changes in capillary perfusion induced by different patterns of activity in rat skeletal muscle Microvascular Research 40 1 1990 14 28
28. C.A. Harms, M.A. Babcock, S.R. McClaran, D.F. Pegelow, G.A. Nickele, and W.B. Nelson Respiratory muscle work compromises leg blood flow during maximal exercise Journal of Applied Physiology 82 5 1997 1573 1583
29. I. Heinonen Comfortable at just below your critical speed: how is blood flow distribution coupled to muscle fibre recruitment during exercise? Journal of Physiology 589 9 2011 2113 2114
30. I. Heinonen, J. Kemppainen, K. Kaskinoro, J.E. Peltonen, R. Borra, M.M. Lindroos, V. Oikonen, P. Nuutila, J. Knuuti, Y. Hellsten, R. Boushel, and K.K. Kalliokoski Comparison of exogenous adenosine and voluntary exercise on human skeletal muscle perfusion and perfusion heterogeneity Journal of Applied Physiology 108 2 2010 378 386
31. I. Heinonen, S.V. Nesterov, J. Kemppainen, P. Nuutila, J. Knuuti, R. Laitio, M. Kjaer, R. Boushel, and K.K. Kalliokoski Role of adenosine in regulating the heterogeneity of skeletal muscle blood flow during exercise in humans Journal of Applied Physiology 103 6 2007 2042 2048
32. A.V. Hill, and H. Lupton Muscular exercise, lactic acid, and the supply and utilization of oxygen The Quart Journal of Medicine 16 1923 135 171
33. H. Hoppeler, and D.L. Turner Plasticity of aerobic scope: adaptation of the respiratory system in animals, organs and cells W. Wieser, E. Gnaiger, Energy transformations in cells and organisms 1998 Thieme Stuttgart, NY 116 122
34. H. Hoppeler, and E.R. Weibel Exercise-induced maximal metabolic rate scales with muscle aerobic capacity Journal of Experimental Biology 208 2005 1635 1644
35. P.O. Iversen, and G. Nicolaysen Heterogeneous blood flow distribution within single skeletal muscles in the rabbit: role of vasomotion, sympathetic nerve activity and effect of vasodilation Acta Physiologica Scandinavica 137 1 1989 125 133
36. P.O. Iversen, M. Standa, and G. Nicolaysen Marked regional heterogeneity in blood flow within a single skeletal muscle at rest and during exercise hyperaemia in the rabbit Acta Physiologica Scandinavica 136 1 1989 17 28
37. R.A. Jacobs, P. Rasmussen, C. Siebenmann, V. Diaz, M. Gassmann, and D. Pesta Determinants of time trial performance and maximal incremental exercise in highly trained endurance athletes Journal of Applied Physiology 111 5 2011 1422 1430
38. K.K. Kalliokoski, J. Kemppainen, K. Larmola, T.O. Takala, P. Peltoniemi, and A. Oksanen Muscle blood flow and flow heterogeneity during exercise studied with positron emission tomography in humans European Journal of Applied Physiology 83 4-5 2000 395 401
39. K.K. Kalliokoski, C. Scheede-Bergdahl, M. Kjaer, and R. Boushel Muscle perfusion and metabolic heterogeneity: insights from non-invasive imaging techniques Exercise and Sport Sciences Review 34 4 2006 164 170
40. 2 supply and utilization in men Journal of Applied Physiology 75 6 1993 2586 2594
41. M.D. Koskolou, J.A. Calbet, G. Radegran, and R.C. Roach Hypoxia and the cardiovascular response to dynamic knee extension exercise American Journal of Physiology 272 2 1997 H2655 H2663
42. A.V. Kuznetsov, R. Guzun, F. Boucher, R. Bagur, T. Kaambre, and V. Saks Mysterious Ca(2+)-independent muscular contraction: déjà vu The Biochemical Journal 445 3 2012 333 336
43. M.H. Laughlin, and R.B. Armstrong Muscular blood flow distribution patterns as a function of running speed in rats American Journal of Physiology 243 2 1982 H296 H306
44. C. Lundby, M. Sander, G. van Hall, B. Saltin, and J.A. Calbet Maximal exercise and muscle oxygen extraction in acclimatizing lowlanders and in high altitude natives The Journal of Physiology 573 2 2006 535 547
45. B.G. Mackie, and R.L. Terjung Influence of training on blood flow to different skeletal muscle fibre types Journal of Applied Physiology 55 4 1983 1072 1078
46. J.H. Mitchell, and B. Saltin The oxygen transport system and maximal oxygen uptake Exercise physiology 2003 Oxford University Press p. 255-91
47. J. McMichael, and E.P. Sharpey-Schafer Cardiac output in man by a direct Fick method: effects of posture, venous pressure change, atropine, and adrenaline British Heart Journal 6 1 1944 33 40
48. S.P. Mortensen, E.A. Dawson, C.C. Yoshiga, M.K. Dalsgaard, R. Damsgaard, and N.H. Secher Limitations to systemic and locomotor limb muscle oxygen delivery and uptake during maximal exercise in humans The Journal of Physiology 166 1 2005 273 285
49. E.A. Newsholme, B. Crabtree, and V.A. Zammit Use of enzyme activities as indices of maximum rates of fuel utilization CIBA Foundation Symposium 73 1980 245 258
50. S.B. Ong, S. Subrayan, S.Y. Lim, D.M. Yellon, S.M. Davidson, and D.J. Hausenloy Inhibiting mitochondrial fission protects the heart against ischemia/reperfusion injury Circulation 121 2010 2012 2022
51. D.R. Pendergast, J.A. Krasney, A. Ellis, B. McDonald, C. Marconi, and P. Cerretelli Cardiac output and muscle blood flow in exercising dogs Respiration Physiology 61 3 1985 317 326
52. C.G. Perry, D.A. Kane, C.T. Lin, R. Kozy, B.L. Cathey, and D.S. Lark Inhibiting myosin ATPase reveals a dynamic range of mitochondrial respiratory control in skeletal muscle The Biochemical Journal 437 2 2011 215 222
53. D. Pesta, and E. Gnaiger High resolution respirometry: OXPHOS protocols for human cells and permeabilized fibres from small biopsies of human muscle Methods in Molecular Biology 810 2012 25 58
54. D. Pesta, F. Hoppel, C. Macek, H. Messner, M. Faulhaber, and C. Kobel Similar qualitative and quantitative changes of mitochondrial respiration following strength and endurance training in nortmoxia and hypoxia in sedentary humans American Journal of Physiology: Regulatory, Integrative and Comparative Physiology 301 4 2011 R1078 R1087
55. M. Picard, T. Taivassalo, G. Gouspillou, and R.T. Hepple Mitochondria: isolation, structure and function Journal of Physiology 589 2011 4413 4421
56. J. Piiper Unequal distribution of blood flow in exercising muscle of the dog Respiration Physiology 80 2-3 1990 129 136
57. 2 transfer in muscle Acta Physiologica Scandinavica 168 4 2000 603 607
58. R.N. Pittman Oxygen transport and exchange in the microcirculation Microcirculation 12 1 2005 59 70
59. G. Rådegran, and J.A. Calbet Role of adenosine in exercise-induced human skeletal muscle vasodilatation Acta Physiologica Scandinavica 171 2 2001 177 185
60. G. Rådegran, and B. Saltin Human femoral artery diameter in relation to knee extensor muscle mass, peak blood flow, and oxygen uptake American Journal of Physiology: Heart and Circulatory Physiology 278 1 2000 H162 H167
61. G. Rådegran, E. Blomstrand, and B. Saltin Peak muscle perfusion and oxygen uptake in humans: importance of precise estimates of muscle mass Journal of Applied Physiology 87 6 1999 2375 2380
62. B. Rasmussen, K. Klausen, J.P. Clausen, and J. Trap-Jensen Pulmonary ventilation, blood gases, and blood pH after training of the arms or the legs Journal of Applied Physiology 38 2 1975 250 256
63. U.F. Rasmussen, H.N. Rasmussen, P. Krustrup, B. Quistorff, B. Saltin, and J. Bangsbo Aerobic metabolism of human quadriceps muscle: in vivo data parallel measurements on isolated mitochondria American Journal of Physiology: Endocrinology and Metabolism 280 2 2001 301 307
64. C.A. Ray, and G.A. Dudley Muscle use during dynamic knee extension: implication for perfusion and metabolism Journal of Applied Physiology 85 3 1998 1194 1197
65. G. Read, B. Crabtree, and G.H. Smith The activities of 2-oxoglutarate dehydrogenase and pyruvate dehydrogenase and pyruvate dehydrogenase in hearts and mammary glands from ruminants and non-ruminants The Biochemical Journal 164 2 1977 349 355
66. R.S. Richardson, B. Kennedy, D.R. Knight, and P.D. Wagner High muscle blood flows are not attenuated by recruitment of additional muscle mass American Journal of Physiology 269 5 Pt 2 1995 H1545 H1552
67. 2 max in the exercise-trained human quadriceps Journal of Applied Physiology 86 3 1999 1048 1053
68. 2 content and tension in regulation of cardiac output and leg blood flow during exercise in humans American Journal of Physiology 276 2 Pt 2 1999 H438 H445
69. T.K. Rostovtseva, L. Kely, K.L. Sheldon, E. Hassanzadeh, C. Monge, and V. Saks Tubulin binding blocks mitochondrial voltage-dependent anion channel and regulates respiration PNAS 105 48 2008 18746 18751
70. V.A. Saks, V.I. Veksler, A.V. Kuznetsov, L. Kay, P. Sikk, and T. Tiivel Permeabilized cell and skinned fibre techniques in studies of mitochondrial function in vivo Molecular and Cellular Biochemistry 184 1-2 1998 81 100
71. V. Saks, R. Guzun, N. Timohhina, K. Tepp, M. Varikmaa, and C. Monge Structure-function relationships in feedback regulation of energy fluxes in vivo in health and disease: mitochondrial interactosome Biochimica et Biophysica Acta 1797 6-7 2010 678 697
72. V.A. Saks, A.V. Kuznetsov, Z.A. Khuchua, E.V. Vasilyeva, J.O. Belikova, and T. Kesvatera Control of cellular respiration in vivo by mitochondrial outer membrane and by creatine kinase. A new speculative hypothesis: possible involvement of mitochondrial-cytoskeleton interactions Journal of Molecular and Cellular Cardiology 27 1 1995 625 645
73. B. Saltin Hemodynamic adaptations to exercise American Journal of Cardiology 55 10 1985 D42 D47
74. B. Saltin, and P.D. Gollnick Skeletal muscle adaptability: significance for metabolism and performance L.D. Peachey, S.R. Geiger, Handbook of physiology: skeletal muscle. Section 10 1983 American Physiological Society/Wilkins and Wilkins Baltimore
75. 2 max is limited primarily by cardiac output and locomotor muscle blood flow Journal of Applied Physiology 100 2 2006 744 748
76. W. Schaffartzik, E.D. Barton, D.C. Poole, K. Tsukimoto, M.C. Hogan, and D.E. Bebout Effect of reduced hemoglobin concentration on leg oxygen uptake during maximal exercise in humans Journal of Applied Physiology 75 2 1993 491 498
77. K. Schwerzmann, H. Hoppeler, S.R. Kayar, and E.R. Weibel Oxidative capacity of muscle and mitochondria: correlation of physiological, biochemical, and morphometric characteristics Proceedings of the National Academy of Sciences of the United States of America 86 1989 1583 1587
78. N.H. Secher, J.P. Clausen, K. Klausen, I. Noer, and J. Trap-Jensen Central and regional circulatory effects of adding arm exercise to leg exercise Acta Physiologica Scandinavica 100 3 1977 288 297
79. W.L. Sexton, and D.C. Poole Costal diaphragm blood flow heterogeneity at rest and during exercise Respiration Physiology 101 2 1995 171 182
80. T.E. Sweeney, and I.H. Sarelius Spatial heterogeneity in striated muscle arteriolar tone, cell flow, and capillarity American Journal of Physiology 259 2 1990 H124 H136
81. C.R. Taylor, and E.R. Weibel Design of the mammalian respiratory system. I. Problem and strategy Respiration Physiology 44 1 1981 1 10
82. M. Tonkonogi, and K. Sahlin Rate of oxidative phosphorylation in isolated mitochondria from skeletal muscle:effect of training status Acta Physiologica Scandinavica 161 1997 345 353
83. I. Vogiatzis, D. Athanasopoulos, R. Boushel, J.A. Guenette, M. Koskolou, and M. Vasilopoulou Contribution of respiratory muscle blood flow to exercise-induced diaphragmatic fatigue in trained cyclists The Journal of Physiology 586 22 2008 5575 5587
84. S. Volianitis, C.C. Yoshiga, P. Nissen, and N.H. Secher Effect of fitness on arm vascular and metabolic responses to upper body exercise American Journal of Physiology: Heart and Circulatory Physiology 286 5 2004 H1736 H1741
85. max at sea level and altitude Respiration Physiology 106 1996 329 343
86. P.D. Wagner Determinants of maximal oxygen transport and utilization Annual Review of Physiology 58 2006 21 50
87. E.R. Weibel, and H. Hoppeler Exercise-induced maximal metabolic rate scales with muscle aerobic capacity Journal of Experimental Biology 208 2005 1635 1644
88. T. Yu, J.L. Robotham, and Y. Yoon Increased production of reactive oxygen species in hyperglycemic conditions requires dynamic change of mitochondrial morphology Proceedings of the National Academy of Sciences of the United States of America 103 2006 2653 2658