Hypoxia refines plasticity of mitochondrial respiration to repeated muscle work

European Journal of Applied Physiology

Volumn 114, Issue 2, 2014, Pages 405-417

  Desplanches, Dominique ^b   Amami, Myriam ^a   Dupré Aucouturier, Sylvie ^b   Valdivieso, Paola ^e   Schmutz, Silvia ^c   Mueller, Matthias ^c   Hoppeler, Hans ^c   Kreis, Roland ^d   Flück, Martin ^a,e  

^a MANCHESTER METROPOLITAN UNIVERSITY   (United Kingdom)

^b CENTRE DE GÉNÉTIQUE MOLÉCULAIRE ET CELLULAIRE   (France)

^c UNIVERSITY OF BERN   (Switzerland)

^d UNIVERSITY OF BERN   (Switzerland)

^e BALGRIST UNIVERSITY HOSPITAL   (Switzerland)

Author keywords

Cytochrome c; Exercise; Gene; Metabolism; Oxygen; Plasticity

Indexed keywords

CYTOCHROME C OXIDASE; MESSENGER RNA; MYOGLOBIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE);

ADULT; ALTITUDE; ANOXIA; ARTICLE; CASE CONTROL STUDY; CELL RESPIRATION; EXERCISE; GENETICS; HUMAN; MALE; METABOLISM; MITOCHONDRION; OXYGEN CONSUMPTION; PHYSIOLOGY; REPERFUSION; SKELETAL MUSCLE; VASCULARIZATION;

ADULT; ALTITUDE; ANOXIA; CASE-CONTROL STUDIES; CELL RESPIRATION; ELECTRON TRANSPORT COMPLEX I; ELECTRON TRANSPORT COMPLEX IV; EXERCISE; HUMANS; MALE; MITOCHONDRIA; MUSCLE, SKELETAL; MYOGLOBIN; OXYGEN CONSUMPTION; REPERFUSION; RNA, MESSENGER;

EID: 84895904912     PISSN: 14396319     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00421-013-2783-8     Document Type: Article

References (45)

1. Adhihetty PJ, Irrcher I, Joseph AM, Ljubicic V, Hood DA (2003) Plasticity of skeletal muscle mitochondria in response to contractile activity. Exp Physiol 88:99-107
2. Ali SS, Hsiao M, Zhao HW, Dugan LL, Haddad GG, Zhou D (2012) Hypoxia-adaptation involves mitochondrial metabolic depression and decreased ROS leakage. PLoS ONE 7:e36801
3. Andrade FH, McMullen CA (2006) Lactate is a metabolic substrate that sustains extraocular muscle function. Pflugers Arch 452:102-108
4. Angermann M, Hoppeler H, Wittwer M, Däpp C, Howald H, Vogt M (2006) Effect of acute hypoxia on maximal oxygen uptake and maximal performance during leg and upper-body exercise in Nordic combined skiers. Int J Sports Med 27:301-306
5. Bakkman L, Sahlin K, Holmberg HC, Tonkonogi M (2007) Quantitative and qualitative adaptation of human skeletal muscle mitochondria to hypoxic compared with normoxic training at the same relative work rate. Acta Physiol (Oxf) 190:243-251
6. Baumgartner I, Thoeny HC, Kummer O, Roefke C, Skjelsvik C, Boesch C, Kreis R (2005) Leg ischemia: assessment with MR angiography and spectroscopy. Radiology 234:833-841
7. Busso T, Fluck M (2013) A mixed-effects model of the dynamic response of muscle gene transcript expression to endurance exercise. Eur J Appl Physiol 113:1279-1290
8. Carlier PG, Bertoldi D, Baligand C, Wary C, Fromes Y (2006) Muscle blood flow and oxygenation measured by NMR imaging and spectroscopy. NMR Biomed 19:954-967
9. Chilibeck PD, Bell GJ, Socha T, Martin T (1998) The effect of aerobic exercise training on the distribution of succinate dehydrogenase activity throughout muscle fibres. Can J Appl Physiol 23:74-86
10. Chilibeck PD, Syrotuik DG, Bell GJ (2002) The effect of concurrent endurance and strength training on quantitative estimates of subsarcolemmal and intermyofibrillar mitochondria. Int J Sports Med 23:33-39
11. Desplanches D, Mayet MH, Sempore B, Flandrois R (1987) Structural and functional responses to prolonged hindlimb suspension in rat muscle. J Appl Physiol 63:558-563
12. Desplanches D, Hoppeler H, Linossier MT, Denis C, Claassen H, Dormois D, Lacour JR, Geyssant A (1993) Effects of training in normoxia and normobaric hypoxia on human muscle ultrastructure. Pflugers Arch 425:263-267
13. Durieux AC, D'Antona G, Desplanches D, Freyssenet D, Klossner S, Bottinelli R, Flück M (2009) Focal adhesion kinase is a load-dependent governor of the slow contractile and oxidative muscle phenotype. J Physiol 587(Pt 14): 3703-3717
14. Elustondo PA, White AE, Hughes ME, Brebner K, Pavlov E, Kane DA (2013) Physical and functional association of lactate dehydrogenase (LDH) with skeletal muscle mitochondria. J Biol Chem 288:25309-25317
15. Fluck M (2006) Functional, structural and molecular plasticity of mammalian skeletal muscle in response to exercise stimuli. J Exp Biol 209:2239-2248
16. Fluckey JD, Ploug D, Galbo H (1999) Mechanisms associated with hypoxia- and contraction-mediated glucose transport in muscle are fibre-dependent. Acta Physiol Scand 167:83-87
17. Flueck M (2009) Plasticity of the muscle proteome to exercise at altitude. High Alt Med Biol 10:183-193
18. Flueck M, Eyeang-Bekale N, Heraud A, Girard A, Gimpl M, Seynnes OR, Rittweger J, Niebauer J, Mueller E, Narici M (2011) Load-sensitive adhesion factor expression in the elderly with skiing: relation to fiber type and muscle strength. Scand J Med Sci Sports 21(Suppl 1):29-38
19. Fukuda R, Zhang H, Kim JW, Shimoda L, Dang CV, Semenza GL (2007) HIF-1 regulates cytochrome oxidase subunits to optimize efficiency of respiration in hypoxic cells. Cell 129:111-122
20. Giraud MN, Fluck M, Zuppinger C, Suter TM (2005) Expressional reprogramming of survival pathways in rat cardiocytes by neuregulin-1beta. J Appl Physiol 99:313-322
21. Green H, Burnett M, Smith I, Tupling S, Ranney D (2009) Failure of hypoxia to exaggerate the metabolic stress in working muscle following short-term training. Am J Physiol 297:R593-R604
22. Hoppeler H, Desplanches D (1992) Muscle structural modifications in hypoxia. Int J Sports Med 13(Suppl 1):S166-S168
23. 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
24. Horowitz JF, Kaufman AE, Fox AK, Harber MP (2005) Energy deficit without reducing dietary carbohydrate alters resting carbohydrate oxidation and fatty acid availability. J Appl Physiol 98:1612-1618
25. Kayar SR, Hoppeler H, Essen-Gustavsson B, Schwerzmann K (1988) The similarity of mitochondrial distribution in equine skeletal muscles of differing oxidative capacity. J Exp Biol 137:253-263
26. Kreis R, Bruegger K, Skjelsvik C, Zwicky S, Ith M, Jung B, Baumgartner I, Boesch C (2001) Quantitative (1)H magnetic resonance spectroscopy of myoglobin de- and reoxygenation in skeletal muscle: reproducibility and effects of location and disease. Magn Reson Med 46:240-248
27. 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
28. Mollard P, Woorons X, Letournel M, Lamberto C, Favret F, Pichon A, Beaudry M, Richalet JP (2007) Determinants of maximal oxygen uptake in moderate acute hypoxia in endurance athletes. Eur J Appl Physiol 100:663-673
29. Perry CG, Lally J, Holloway GP, Heigenhauser GJ, Bonen A, Spriet LL (2010) Repeated transient mRNA bursts precede increases in transcriptional and mitochondrial proteins during training in human skeletal muscle. J Physiol 588:4795-4810
30. Pilegaard H, Ordway GA, Saltin B, Neufer PD (2000) Transcriptional regulation of gene expression in human skeletal muscle during recovery from exercise. Am J Physiol 279:E806-E814
31. Pilegaard H, Saltin B, Neufer PD (2003) Exercise induces transient transcriptional activation of the PGC-1alpha gene in human skeletal muscle. J Physiol 546:851-858
32. Ponsot E, Dufour SP, Zoll J, Doutrelau S, N'Guessan B, Geny B, Hoppeler H, Lampert E, Mettauer B, Ventura-Clapier R, Richard R (2006) Exercise training in normobaric hypoxia in endurance runners. II. Improvement of mitochondrial properties in skeletal muscle. J Appl Physiol 100:1249-1257
33. Quinlan CL, Orr AL, Perevoshchikova IV, Treberg JR, Ackrell BA, Brand MD (2012) Mitochondrial complex II can generate reactive oxygen species at high rates in both the forward and reverse reactions. J Biol Chem 287:27255-27264
34. 2 transport. J Clin Invest 96:1916-1926
35. 2 assessed by myoglobin desaturation: response to graded exercise. J Appl Physiol 91:2679-2685
36. Schmutz S, Dapp C, Wittwer M, Vogt M, Hoppeler H, Fluck M (2006) Endurance training modulates the muscular transcriptome response to acute exercise. Pflugers Arch 451:678-687
37. Schmutz S, Dapp C, Wittwer M, Durieux AC, Mueller M, Weinstein F, Vogt M, Hoppeler H, Flueck M (2010) A hypoxia complement differentiates the muscle response to endurance exercise. Exp Physiol 95:13
38. Scott GR, Egginton S, Richards JG, Milsom WK (2009) Evolution of muscle phenotype for extreme high altitude flight in the bar-headed goose. Proc Biol Sci 276:3645-3653
39. Slotboom J, Boesch C, Kreis R (1998) Versatile frequency domain fitting using time domain models and prior knowledge. Magn Reson Med 39:899-911
40. Terrados N, Jansson E, Sylvén C, Kaijser L (1990) Is hypoxia a stimulus for synthesis of oxidative enzymes and myoglobin? J Appl Physiol 68:2369-2372
41. Tevald MA, Lanza IR, Befroy DE, Kent-Braun JA (2009) Intramyocellular oxygenation during ischemic muscle contractions in vivo. Eur J Appl Physiol 106:333-343
42. Vogt M, Puntschart A, Geiser J, Zuleger C, Billeter R, Hoppeler H (2001) Molecular adaptations in human skeletal muscle to endurance training under simulated hypoxic conditions. J Appl Physiol 91:173-182
43. Wagner PD (2012) Muscle intracellular oxygenation during exercise: optimization for oxygen transport, metabolism, and adaptive change. Eur J Appl Physiol 112:1-8
44. Wiesner S, Haufe S, Engeli S, Mutschler H, Haas U, Luft FC, Jordan J (2010) Influences of normobaric hypoxia training on physical fitness and metabolic risk markers in overweight to obese subjects. Obesity (Silver Spring) 18:116-120
45. Zoll J, Ponsot E, Dufour S, Doutreleau S, Ventura-Clapier R, Vogt M, Hoppeler H, Richard R, Fluck M (2006) Exercise training in normobaric hypoxia in endurance runners. III. Muscular adjustments of selected gene transcripts. J Appl Physiol 100:1258-1266