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Rate of oxidative phosphorylation in isolated mitochondria from human skeletal muscle: effect of training status
Abstract
Muscle oxidative function has been investigated in subjects with various training status (VO2 max, 41-72 mL O2 kg-1 body wt min-1, n = 10). Mitochondria were isolated from biopsies taken from m. vastus lateralis. Maximal mitochondrial oxygen consumption (QO2) and ATP production (MAPR) were measured with polarographic and bioluminometric techniques, respectively. The yield of mitochondria, calculated from the fractional activity of citrate synthase (CS), averaged 26%. With pyruvate + malate, the respiratory control ratio was 5.7 +/- 0.4 (X +/- SE) and the P/O ratio was 2.83 +/- 0.02, which demonstrates that the isolated mitochondria were functionally intact. QO2 was significantly correlated to aerobic training status expressed as muscle CS activity (r = 0.86), VO2 max (r = 0.84) and lactate threshold (r = 0.83) but not to the fibre type composition. A highly significant correlation (r = 0.93) was observed between ATP production calculated from QO2 and MAPR, but ATP production derived from QO2 was higher than MAPR both for pyruvate + malate (255%) and for alpha-ketoglutarate (23%). QO2 extrapolated to a temperature of 38 degrees C averaged 68 mL O2 min-1 kg-1 wet wt, which is similar to previous findings in vitro and in vivo during the post-exercise period. However, calculated muscle O2 utilization during exercise was three- to fivefold higher than QO2 measured on isolated mitochondria. It is suggested that additional factors exist for activation of mitochondrial respiration during exercise. It is concluded that muscle oxidative function can be quantitatively assessed from the respiration of mitochondria isolated from needle biopsy specimens and that QO2 is closely correlated to whole-body VO2 max.
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“The fact that we were able to demonstrate this impairment in OXPHOS capacity (complex I and II substrates combined) in the patients even at these relatively low flux rates, emphasizes the potential of our finding (in vivo flux rates are much higher than these ex vivo flux rates [38]).”
From Simvastatin Effects on Skeletal Muscle (2013) · cites this paper as [38]
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“Rat brain mitochondria were isolated as described by Tonkonogi and Sahlin (1997) with some modifications.”
MethodHey‐Mogensen, M., Jeppesen, J. F., Madsen, K., Kiens, B., & Franch, J. (2011) · Acta Physiologica · doi:10.1111/j.1748-1716.2011.02347.x · Cited by 28
“Mitochondria were isolated according to a technique previously described in detail (Tonkonogi & Sahlin 1997).”
MethodEffect of Lipid Infusion on Metabolism and Force of Rat Skeletal Muscles During Intense Contractions
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“In intact skeletal muscle the maximal V̇O2 is two to six times greater than in isolated mitochondria (18, 25, 27).”
BackgroundCryotherapy reduces skeletal muscle damage after ischemia/reperfusion in rats
Puntel, G. O., de Carvalho, N. R., Dobrachinski, F., et al. (2012) · Journal of Anatomy · doi:10.1111/joa.12009 · Cited by 25
“Isolation of skeletal muscle mitochondria: rat skeletal muscle mitochondria were isolated as described by Tonkonogi & Salhin (1997), with some modifications.”
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“Address for reprint requests and other correspondence: K. Sahlin, Dept. of Physiology and Pharmacology, Karolinska Institute, Box 5626, S-11486 Stockholm, Sweden (E-mail: kent.sahlin@fyfa.ki.se).”
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“Mitochondrial yield was calculated as a percent of CS activity in isolated mitochondria compared to whole homogenate [Tonkonogi and Sahlin, 1997].”
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“In addition to the pumping capacity of the heart, mitochondrial number (or volume) in the skeletal muscle is closely correlated with aerobic capacity (52, 59).”
Background‘Idealized’ State 4 and State 3 in Mitochondria vs. Rest and Work in Skeletal Muscle
Korzeniewski, B. (2015) · PLoS ONE · doi:10.1371/journal.pone.0117145 · Cited by 25
“In other words, the scaling factor between muscle wet weight and mitochondrial protein content is about 18 g mitochondrial protein per 1 kg of wet muscle weight [40] (assuming that proteins constitute about 25% of mitochondria).”
BackgroundResultInfluentialEffect of Novel Antipsychotics on Energy Metabolism — In Vitro Study in Pig Brain Mitochondria
Ľupták, M., Fišar, Z., & Hroudová, J. (2021) · Molecular Neurobiology · doi:10.1007/s12035-021-02498-4 · Cited by 23
Biochemical Background of the VO2 On-Kinetics in Skeletal Muscles
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Reduced glucose tolerance and insulin sensitivity after prolonged exercise in endurance athletes
Flockhart, M., Tischer, D., Nilsson, L. C., Blackwood, S. J., Ekblom, B. T., Katz, A., Apró, W., & Larsen, F. J. (2023) · Acta Physiologica · doi:10.1111/apha.13972 · Cited by 26
“Isolation of mitochondria was performed as previously described 74 with modifications.”
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“The positive correlation between the muscle’s oxidative capacity and VO 2 max is well established (Jacobs & Lundby, 2013; Larson-Meyer et al., 2000; Tonkonogi & Sahlin, 1997; Zoll et al., 2002).”
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“This connection may be based on the facts that rate of oxidative phosphorylation from human skeletal muscle is in very close correlation with VO 2max58,59 .”
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“…also peripheral limitations (di Prampero, 2003), a link between V̇O2max and lactate recovery could be explained by lactate removal increasing with a higher maximal oxidative capacity (Thomas, Sirvent, Perrey, Raynaud, & Mercier, 2004), which is closely related to V̇O2max (Tonkonogi & Sahlin, 1997).”
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“The respiratory data from the present study agree with the general mitochondrial respiratory improvement in aerobically trained muscles largely reported both in humans and animals (Holloszy, 1967; Tonkonogi and Sahlin, 1997; Tonkonogi et al., 2000a,b; Walsh et al., 2001; Zoll et al., 2002; Garnier et al., 2005; Daussi…”
BackgroundResultSahlin, K., Nielsen, J. S., Mogensen, M., & Tonkonogi, M. (2006) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01007.2005 · Cited by 14
“CS activity was measured spectrophotometrically (25°C) in isolated mitochondria and in freeze-dried muscle and dissected free from nonmuscle constituents, using a technique described previously (37).”
MethodSelf-citationReaction–diffusion constraints in living tissue: Effectiveness factors in skeletal muscle design
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A novel method for determining human ex vivo submaximal skeletal muscle mitochondrial function
Hey‐Mogensen, M., Gram, M., Jensen, M. B., Lund, M. T., HANSEN, C. N., Scheibye‐Knudsen, M., Bohr, V. A., & Dela, F. (2015) · The Journal of Physiology · doi:10.1113/jp270204 · Cited by 14
“The major part of the muscle biopsy was used for mitochondrial isolation as described previously (Tonkonogi & Sahlin, 1997) using protease (0.2 mg ml−1 protease; Subtilisin Carlsberg; EC 232-752-2, type VIII; Sigma, St Louis, MO, USA) and different centrifugation steps to isolate the mitochondria…”
MethodInfluentialCoronary and muscle blood flow during physical exercise in humans; heterogenic alliance
Zoladz, J. A., Majerczak, J., Duda, K., & Chłopicki, S. (2015) · Pharmacological Reports · doi:10.1016/j.pharep.2015.06.002 · Cited by 14
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“MiR05 buffer was used as the medium, the same substrate mixture as above was added, 230 μL of luciferase reagent was added and ATP kinetics was measured using the luminescence (measured for 4 min) [42].”
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“On the other hand, it was proposed that during whole body exercise, the oxygen transport is limiting for the maximal oxygen uptake in working muscles (VO2m,max) and in lungs (VO2p,max) (34, 38, 39), and therefore the maximal oxygen consumption per muscle mass is significantly greater during single-muscle exercise (350…”
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“Given that increases in mitochondrial parameters (citrate synthase activity and respiration) coincide with a whole-body increase in _ VO2max [2, 5, 6], one can suppose that a combination of low-intensity and high-intensity exercise increases mitochondria biogenesis.”
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MethodResultInfluentialKhemraj, P., Kuznyetsova, A., & Hood, D. A. (2025) · Journal of sport and health science/Journal of Sport and Health Science · doi:10.1016/j.jshs.2025.101049 · Cited by 14
“48,49”
Mitochondrial respiration of complex II is not lower than that of complex I in mouse skeletal muscle
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Brands, M., Verhoeven, A. J., & Serlie, M. J. M. (2011) · Advances in experimental medicine and biology · doi:10.1007/978-94-007-2869-1_9 · Cited by 9
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Mitochondrial Coupling and Contractile Efficiency in Humans with High and Low V˙O2peaks
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“In contrast, during exercise or ADP-stimulated respiration, mitochondrial coupling would be optimized for ATP synthesis regardless of the muscle aerobic capacity as suggested here in vivo and previously in vitro (34,42,43).”
BackgroundPremedication with pioglitazone prevents doxorubicin-induced left ventricular dysfunction in mice
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“…flux rates that can be achieved in the present ex vivo system are only a fraction of what is seen in vivo where oxygen utilization is 2.5–5 times higher than what can be measured in vitro and ex vivo [for quantitative considerations of this issue, see (Tonkonogi & Sahlin 1997) and (Gnaiger 2009)].”
BackgroundInfluentialThe effect of plasma from septic ICU patients on healthy rat muscle mitochondria
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“In the first experiment, mitochondria were isolated according as described before [14].”
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“The Wistar rats were sacrificed through cervical dislocation before hindlimb muscles were removed for the isolation of mitochondria by a modified method of Tonkonogi and Sahlin (1997).”
MethodGranata, C., Caruana, N. J., Botella, J., Jamnick, N. A., Huynh, K., Kuang, J., Janssen, H. A., Reljić, B., Mellett, N. A., Laskowski, A., et al. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.02.19.431993 · Cited by 6
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“The activity of citrate synthase was measured spectrophotometrically according to Tonkonogi and Sahlin (1997) as a consumption of oxalacetate, which leads to reduction of NAD.”
MethodMitochondrial disorders and exertional intolerance: Controversy continues
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“3) are somewhat lower than the P/O2 value that can be found in research papers and textbooks (i.e. 6) and of the P/O ratio of about 2.83 which has been determined on isolated mitochondria extracted from human skeletal muscle (Tonkonogi and Sahlin 1997).”
BackgroundInfluentialAdaptation of Skeletal Muscle Mass and Metabolism to Physical Exercise
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“This step is adapted from the protocol described in (Tonkonogi and Sahlin, 1997)”
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“…endurance trained individuals, who through years of training already possess highly adapted physiology, including capillary to fibre ratios and oxidative enzyme activities double that of untrained individuals (Hermansen & Wachtlova, 1971; Ingjer, 1979; Saltin et al. 1977; Tonkonogi & Sahlin, 1997).”
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“In previous study focusing on ATP synthesis capacity, the ATP production rate correlated to endurance capacity (Tonkonogi & Sahlin 1997), and endurance training increased the ability of ATP production (Wibom, et al., 1992; Starritt, et al., 1999).”
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Self-citationbred for high aerobic capacity Enhanced mitochondrial sensitivity to creatine in rats
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Nielsen, T. P., Damgaard, M., Andersen, N. R., Dunø, M., Frederiksen, A. L., van Hall, G., Sylow, L., Murgia, M., Larsen, S., Torekov, S. S., et al. (2025) · medRxiv · doi:10.64898/2025.12.17.25342274
Arieta, L. R., Smith, Z. H., Nagarajan, R., Meyerspeer, M., & Kent, J. A. (2026) · The Journal of Physiology · doi:10.1113/jp291176
“…of ∼ 1.64 obtained in this study are roughly similar to previous studies that have quantified P/O in human skeletal muscle using both in vivo (Amara et al., 2007; Erol et al., 2025; Johannsen et al., 2012; Sparks et al., 2016) and in vitro (Max et al., 1972; Tonkonogi & Sahlin, 1997) measurements.”
InfluentialMaximal Oxygen Uptake (VO2max)
Zoladz, J. A., & Grassi, B. (2026) · Springer eBooks · doi:10.1007/978-3-032-05988-8_127
Korzeniewski, B. (2026) · European Journal of Applied Physiology · doi:10.1007/s00421-026-06365-9
“In human skeletal muscle, V̇ O 2max is significantly higher and equals about 15–16 mM min −1 and V̇ O 2 increases several ten times in relation to rest (Saltin 1985; Andersen and Saltin 1985; Richardson et al. 1995; Blomstrand et al. 1997 ; Tonkonogi and Sahlin 1997 ).”
Citius, Maius, Melius: Mitochondria and Endurance Performance
Botella, J., Bishop, D. J., & Granata, C. (2026) · Sports Medicine · doi:10.1007/s40279-026-02530-4
Metadata
- Authors
- TONKONOGI, M., & SAHLIN, K.
- Affiliations
- Karolinska Institutet (SE)
- Corresponding author
- SAHLIN, K.
- Venue
- Acta Physiologica Scandinavica
- Publisher
- Wiley
- Published
- 1997-10
- Volume
- 161
- Issue
- 3
- Pages
- 345-353
- ISSN
- 0001-6772 (ISSN-L)
- 1365-201X
- OpenAlex
- W2146665077
- Cited by
- 184
- References
- 0
- Citations by year
- 2026: 4 · 2025: 4 · 2024: 2 · 2023: 7 · 2022: 4 · 2021: 11 · 2020: 1 · 2019: 5 · 2018: 5 · 2017: 2 · 2016: 4 · 2015: 12 · 2014: 5 · 2013: 9 · 2012: 9
- FWCI
- 7.31
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Acta Physiologica Scandinavica (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Physiology (medical) › Cardiovascular and exercise physiology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
- Health Sciences › Medicine › Physiology (medical) › Exercise and Physiological Responses
- Keywords
- oxidative phosphorylation, skeletal muscle mitochondria, mitochondrial oxygen consumption, ATP production, citrate synthase, respiratory control ratio, P/O ratio, vastus lateralis, VO2max, lactate threshold, muscle fiber composition
- MeSH terms
- Adenosine Triphosphate, Adult, Aerobiosis, Citrate (si)-Synthase, Humans, Luminescent Measurements, Male, Mitochondria, Muscle, Oxidative Phosphorylation, Oxygen Consumption, Physical Fitness, Muscle, Skeletal, Muscle Fibers, Skeletal
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