Mitochondrial Physiology Network 10.9: 16 (2005) - download pdf

Local adaptations in mitochondrial substrate-specific O₂ flux capacity with prolonged, low intensity, whole-body endurance training.

Robert Boushel¹, C Wright-Paradis¹, H Sondergaard², JA Calbet³, B Saltin², J Helge², E Gnaiger⁴

¹Dept. Exercise Science, Concordia University, Montreal, Canada; ²Copenhagen Muscle Research Centre, Denmark; ³Dept. Physical Education, University Las Palmas, Gran Canaria, Spain; ⁴D. Swarovski Research Lab., Dept. Transplant Surgery, Innsbruck Medical University, Austria. - boushel@alcor.concordia.ca

    Endurance training elevates peak muscle oxygen uptake by means of hemodynamic increases in oxygen delivery and local increases in muscle capillary and mitochondrial density. In addition, training enhances the rate of muscle fat oxidation for energy supply during submaximal exercise [1]. The purpose of this study was to investigate the temporal adaptations in whole body and local arm and leg muscle oxidative capacity and substrate utilization at several stages of low intensity endurance training. Seven healthy Danes skied for 6 hours daily at 65 % of maximum heart rate over 42 days in the polar region of northern Greenland. High-resolution respirometry (Oroboros Oxygraph-2k) allowed quantification of mitochondrial respiratory capacities from saponin-permeabilized skeletal fibers (2-6 mg) of the deltoid and vastus muscles [2].

    At baseline, state 3 O₂ flux (in the presence of ADP) with parallel electron input into complexes I+II (glutamate, malate and succinate) was higher in the vastus compared to the deltoid (54 ±7 vs. 37±2 pmol∙s∙^-1mg^-1, respectively; P<.05). At training day 7, state 3 phosphorylation capacity was unchanged in the deltoid but reduced to 31±5 pmol∙s^-1∙mg^-1 in the vastus (P<.05). After 42 days of skiing, flux capacity was the same in both muscles (38±3 pmol∙s^-1∙mg^-1). State 3 O₂ flux with octanoylcarnitine+malate was also higher in the vastus compared to deltoid at baseline (13±0.5 vs 10±0.5 pmol∙s^-1∙mg^-1, respectively; P<.05), but after 42 days of skiing both muscles had equal flux capacity with fat substrate (12.3±0.8 vs. 12.7±1 pmol∙s^-1∙mg^-1). Despite a daily energy expenditure of ~25,000 kJ (~6,000 kcal) over the 42 day ski sojourn, there were no changes in muscle mass, whole body V_O2max or substrate utilization measured by whole body respiratory quotient, nor whole-leg and arm V_O2max.

    These data reflect that (1) prolonged low intensity endurance exercise induces local adaptations to equalize substrate-specific muscle phosphorylation capacity preferentially towards energy sustainability rather than for peak respiratory power, and (2) high-resolution respirometry provides insight into local, muscle-specific adaptations not detectable with whole body or limb measures of oxidative capacity or substrate utilization. Considering previous findings indicating that mitochondrial function is not a limiting factor for V_O2max, these local muscle adaptations support the novel concept of exercise-specific muscle ‘metabolic fitness’. In addition to the importance of cardiovascular fitness, these findings may have important implications for health.

Supported by Fonds de la Recherche en Sante Quebec (FRSQ), Concordia University, The Natural Science and Engineering Research Council of Canada (NSERC) and the Copenhagen Muscle Research Centre.

1.    Helge JW, Lundby C, Christensen DL, Langfort J, Messonnier L, Zacho M, Andersen JL, Saltin B (2003) Skiing across the Greenland icecap: divergent effects on limb muscle adaptations and substrate oxidation. J. Exp. Biol. 206: 1075-1083.

2.  Kuznetsov AV, Schneeberger S, Seiler R, Brandacher G, Mark W, Steurer W, Saks V, Usson Y, Margreiter R, Gnaiger E (2004) Mitochondrial defects and heterogeneous cytochrome c release after cardiac cold ischemia and reperfusion. Am. J. Physiol. Heart Circ. Physiol. 286: H1633–H1641.