Cited by 185Cardiovascular and exercise physiologyMitochondrial Function and PathologyExercise and Physiological Responses

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Rate of oxidative phosphorylation in isolated mitochondria from human skeletal muscle: effect of training status

TONKONOGI, M., SAHLIN, K.·1997·Acta Physiologica Scandinavica

DOI 10.1046/j.1365-201x.1997.00222.x

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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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Psilander, N., Wang, L., Westergren, J., Tonkonogi, M., & Sahlin, K. (2010) · European Journal of Applied Physiology · doi:10.1007/s00421-010-1544-1 · Cited by 66
“Muscle oxidative power correlates strongly with aerobic training status and endurance performance (Holloszy 1967; Irrcher et al. 2003; Tonkonogi and Sahlin 1997 ).”
BackgroundMethodSelf-citation
Skeletal muscle mitochondrial ATP production rate and walking performance in peripheral arterial disease
Hou, X., Green, S., Askew, C. D., Barker, G. A., Green, A., & Walker, P. J. (2002) · Clinical Physiology and Functional Imaging · doi:10.1046/j.1475-097x.2002.00423.x · Cited by 62
“…as it applies to human muscle tissue was developed by Wibom et al. (Wibom & Hultman, 1990; Wibom et al., 1992) and applied in the present study as well as by others in human exercise-related studies (Berthon et al., 1995; Tonkonogi & Sahlin, 1997; Starritt et al., 1999; Tonkonogi et al., 1999).”
BackgroundResult
Redox State of Endogenous Coenzyme Q Modulates the Inhibition of Linoleic Acid-Induced Uncoupling by Guanosine Triphosphate in Isolated Skeletal Muscle Mitochondria
Jarmuszkiewicz, W., Navet, R., Alberici, L. C., Douette, P., Sluse‐Goffart, C. M., Sluse, F. E., & Vercesi, A. E. (2004) · Journal of Bioenergetics and Biomembranes · doi:10.1023/b:jobb.0000047331.25248.7a · Cited by 59
Human quadricepts muscle mitochondria: A functional characterization
Rasmussen, U. F., & Rasmussen, H. (2000) · Molecular and Cellular Biochemistry · doi:10.1023/a:1007046028132 · Cited by 55
“This muscle is known to be very homogenous with about 55% type I oxidative fibres and the content of connective tissue is modest [17].”
Background
Endurance training increases stimulation of uncoupling of skeletal muscle mitochondria in humans by non-esterified fatty acids: an uncoupling-protein-mediated effect?
Tonkonogi, M., Krook, A., Walsh, B. J., & Sahlin, K. (2000) · Biochemical Journal · doi:10.1042/bj3510805 · Cited by 60
Self-citation
The potential for mitochondrial fat oxidation in human skeletal muscle influences whole body fat oxidation during low-intensity exercise
Sahlin, K., Mogensen, M., Bagger, M., Fernström, M., & Pedersen, P. K. (2006) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00266.2006 · Cited by 57
“The remaining part (100–250 mg) was weighed and used for mitochondrial isolation as described previously (48).”
MethodSelf-citation
Sodium bicarbonate ingestion prior to training improves mitochondrial adaptations in rats
Bishop, D. J., Thomas, C., Moore-Morris, T., Tonkonogi, M., Sahlin, K., & Mercier, J. G. (2010) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00738.2009 · Cited by 52
“increases in Vmax with endurance training (14, 53, 59).”
BackgroundSelf-citation
Abnormal Transition Pore Kinetics and Cytochrome C Release in Muscle Mitochondria of Patients with Chronic Obstructive Pulmonary Disease
Puente‐Maestu, L., Pérez-Parra, J., Mayoral, R. G., Moreno‐Mata, N., Tejedor, A., Torres, A., Lázaro, A., Ferreira, A., & Agustí, A. G. N. (2008) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/rcmb.2008-0289oc · Cited by 54
“However, we isolated mitochondria using well established techniques (27, 33), both in patients and in control subjects.”
BackgroundMethod
Therapeutic cold: An effective kind to modulate the oxidative damage resulting of a skeletal muscle contusion
Puntel, G. O., de Carvalho, N. R., Amaral, G. P., Lobato, L. D., Silveira, S. O., Daubermann, M. F., Barbosa, N. V., da Rocha, J. B. T., & Soares, F. A. A. (2010) · Free Radical Research · doi:10.3109/10715762.2010.517252 · Cited by 52
Linoleic acid improves assembly of the CII subunit and CIII2/CIV complex of the mitochondrial oxidative phosphorylation system in heart failure
Maekawa, S., Takada, S., Nambu, H., Furihata, T., Kakutani, N., Setoyama, D., Ueyanagi, Y., Kang, D., Sabe, H., & Kinugawa, S. (2019) · Cell Communication and Signaling · doi:10.1186/s12964-019-0445-0 · Cited by 51
Regulation of oxidative phosphorylation in intact mammalian heart in vivo
Korzeniewski, B., Noma, A., & Matsuoka, S. (2005) · Biophysical Chemistry · doi:10.1016/j.bpc.2005.04.001 · Cited by 51
In vivo oxidative capacity varies with muscle and training status in young adults
Larsen, R. G., Callahan, D. M., Foulis, S. A., & Kent‐Braun, J. A. (2009) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00260.2009 · Cited by 50
Theoretical studies on the regulation of oxidative phosphorylation in intact tissues
Korzeniewski, B. (2001) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/s0005-2728(00)00237-1 · Cited by 49
Erythropoietin Treatment Enhances Muscle Mitochondrial Capacity in Humans
Plenge, U., Belhage, B., Guadalupe‐Grau, A., Andersen, P. R., Lundby, C., Dela, F., Stride, N. O., Pott, F. C., Helge, J. W., & Boushel, R. (2012) · Frontiers in Physiology · doi:10.3389/fphys.2012.00050 · Cited by 47
“Traditionally it has been thought that increases in mitochondrial respiratory capacity result from an enlargement of mitochondrial volume rather than by altered intrinsic capacity of mitochondria (Holloszy, 1967; Reichmann et al., 1985; Tonkonogi and Sahlin, 1997; Tonkonogi et al., 1997, 2000).”
Background
AMP Deamination Delays Muscle Acidification during Heavy Exercise and Hypoxia
Korzeniewski, B. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m510418200 · Cited by 48
Both linoleic and α-linolenic acid prevent insulin resistance but have divergent impacts on skeletal muscle mitochondrial bioenergetics in obese Zucker rats
Matravadia, S., Herbst, E. A. F., Jain, S. S., Mutch, D. M., & Holloway, G. P. (2014) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00032.2014 · Cited by 46
“The respective speeds of centrifugation at each step were adapted from previous work (11) as well as the chemical composition of the isolation buffer (52).”
Method
Mitochondrial efficiency in rat skeletal muscle: influence of respiration rate, substrate and muscle type
Mogensen, M., & Sahlin, K. (2005) · Acta Physiologica Scandinavica · doi:10.1111/j.1365-201x.2005.01488.x · Cited by 45
“Mitochondria were isolated with a technique previously described in detail (Tonkonogi & Sahlin 1997).”
MethodResultSelf-citation
Perturbations of NAD+salvage systems impact mitochondrial function and energy homeostasis in mouse myoblasts and intact skeletal muscle
Agerholm, M., Dall, M., Jensen, B. A. H., Prats, C., Madsen, S., Basse, A. L., Graae, A.-S., Risis, S., Goldenbaum, J., Quistorff, B., et al. (2017) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00213.2017 · Cited by 42
Quantitative and qualitative adaptation of human skeletal muscle mitochondria to hypoxic compared with normoxic training at the same relative work rate
Bakkman, L., Sahlin, K., Holmberg, H., & Tonkonogi, M. (2007) · Acta Physiologica · doi:10.1111/j.1748-1716.2007.01683.x · Cited by 44
“The remaining part (about 2007 Scandinavian Physiological Society, doi: 10.1111/j.1748-1716.2007.01683.x 245 100 mg) was used for isolation of mitochondria according to Tonkonogi & Sahlin (1997).”
MethodInfluentialSelf-citation
Mitochondrial function in liver cells is resistant to perturbations in NAD+ salvage capacity
Dall, M., Trammell, S. A. J., Asping, M., Hassing, A. S., Agerholm, M., Vienberg, S. G., Gillum, M. P., Larsen, S., & Treebak, J. T. (2019) · Journal of Biological Chemistry · doi:10.1074/jbc.ra118.006756 · Cited by 40
Ex vivo measures of muscle mitochondrial capacity reveal quantitative limits of oxygen delivery by the circulation during exercise
Boushel, R., & Saltin, B. (2012) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2012.09.024 · Cited by 41
Reduced Respiratory Capacity in Muscle Mitochondria of Obese Subjects
Bakkman, L., Fernström, M., Loogna, P., Rooyackers, O., Brandt, L., & Lagerros, Y. T. (2010) · Obesity Facts · doi:10.1159/000320167 · Cited by 34
FAT/CD36 is localized in sarcolemma and in vesicle-like structures in subsarcolemma regions but not in mitochondria
Jeppesen, J. F., Mogensen, M., Prats, C., Sahlin, K., Madsen, K., & Kiens, B. (2009) · Journal of Lipid Research · doi:10.1194/jlr.m003756 · Cited by 33
Self-citation
Enhanced mitochondrial sensitivity to creatine in rats bred for high aerobic capacity
Walsh, B. J., Hooks, R. B., Hornyak, J. E., Koch, L. G., Britton, S. L., & Hogan, M. C. (2006) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01533.2005 · Cited by 35
“These qualitative alterations include an increased maximal ATP production rate via fatty acids compared with other substrates (38), decreased sensitivity of the mitochondrion to ADP (ADP sensitivity) (31, 36), and an enhanced ability of creatine (Cr) to further increase the rate of submaximally ADP-stimulated respirat…”
Background
Lifelong Physical Activity Modulation of the Skeletal Muscle Mitochondrial Proteome in Mice
Alves, R. M. P., Vitorino, R. M. P., Figueiredo, P., Duarte, J. A., Ferreira, R. M., & Amado, F. M. L. (2010) · The Journals of Gerontology Series A · doi:10.1093/gerona/glq081 · Cited by 35
Metabolic control over the oxygen consumption flux in intact skeletal muscle: in silico studies
Liguzinski, P., & Korzeniewski, B. (2006) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00078.2006 · Cited by 35
“tonmotive force ( p) during rest-to-work transition (26, 27), the much steeper phenomenological V̇O2/[ADP] relationship in intact skeletal muscle than in isolated muscle mitochondria (26, 27), the two to five (to seven) times greater maximum oxygen consumption in intact human skeletal muscle than in isolated mitochond…”
Background
Vitamin E prevents hypobaric hypoxia-induced mitochondrial dysfunction in skeletal muscle
Magalhães, J., Ferreira, R. M., Neuparth, M. J., Oliveira, P. J., Marques, F., & Ascensão, A. A. M. R. (2007) · Clinical Science · doi:10.1042/cs20070075 · Cited by 34
“Skeletal muscle mitochondria were prepared by conventional methods involving differential centrifugation, as previously described by Tonkonogi and Sahlin [18].”
Method
Evaluation of quantitative and qualitative aspects of mitochondrial function in human skeletal and cardiac muscles
N’guessan, B. B., Zoll, J., Ribera, F., Ponsot, E., Lampert, E., Ventura‐Clapier, R., Veksler, V., & Mettauer, B. (2003) · Molecular and Cellular Biochemistry · doi:10.1023/b:mcbi.0000009874.14649.ca · Cited by 33
“The fact that values of oxygen consumption when extrapolated from ex vivo experiments are usually lower than those measured in vivo have often been discussed in the literature [46, 47].”
Background
Tissue Specific Phosphorylation of Mitochondrial Proteins Isolated from Rat Liver, Heart Muscle, and Skeletal Muscle
Bak, S. Y., León, I. R., Jensen, O. N., & Højlund, K. (2013) · Journal of Proteome Research · doi:10.1021/pr400281r · Cited by 33
Dietary α-linolenic acid supplementation alters skeletal muscle plasma membrane lipid composition, sarcolemmal FAT/CD36 abundance, and palmitate transport rates
Chorner, Z., Barbeau, P., Castellani, L. N., Wright, D. C., Chabowski, A., & Holloway, G. P. (2016) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00346.2016 · Cited by 32
Mitochondrial Plasticity with Exercise Training and Extreme Environments
Boushel, R., Lundby, C., Qvortrup, K., & Sahlin, K. (2014) · Exercise and Sport Sciences Reviews · doi:10.1249/jes.0000000000000025 · Cited by 32
“This pattern is consistent with several longitudinal studies showing an increase in OXPHOS after training proportionate with enhanced mitochondrial volume density (18,19,38).”
BackgroundResultInfluentialSelf-citation
Regulation of oxidative phosphorylation through each-step activation (ESA): Evidences from computer modeling
Korzeniewski, B. (2016) · Progress in Biophysics and Molecular Biology · doi:10.1016/j.pbiomolbio.2016.12.001 · Cited by 33
“Indeed, the maximal _VO2 (recalculated for mitochondrial proteins) is 2.5e5 times (or more) greater in intact skeletal muscle than in isolated skeletal muscle mitochondria (Tonkonogi and Sahlin, 1997; Korzeniewski and Zoladz, 2001; Korzeniewski, 2014, 2015a; Korzeniewski and Rossiter, 2015).”
BackgroundInfluential
Cold-water immersion following sprint interval training does not alter endurance signaling pathways or training adaptations in human skeletal muscle
Broatch, J. R., Petersen, A. C., & Bishop, D. J. (2017) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00434.2016 · Cited by 36
“Located exclusively in the mitochondria (65), CS is an enzyme commonly used in exercise-training studies as a biomarker of mitochondrial content (11, 38).”
Method
Improvement of Physical Decline Through Combined Effects of Muscle Enhancement and Mitochondrial Activation by a Gastric Hormone Ghrelin in Male 5/6Nx CKD Model Mice.
Tamaki, M., Hagiwara, A., Miyashita, K., Wakino, S., Inoue, H., Fujii, K., Fujii, C., Sato, M., Mitsuishi, M., Muraki, A., et al. (2015) · Endocrinology · doi:10.1210/en.2015-1353 · Cited by 33
Mitochondrial function in metabolic health: A genetic and environmental tug of war
Stephenson, E. J., & Hawley, J. A. (2013) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2013.12.004 · Cited by 28
Differential effects of endurance training and creatine depletion on regional mitochondrial adaptations in rat skeletal muscle
Roussel, D., Lhenry, F., Ecochard, L., SEMPORE, B., Rouanet, J., & Favier, R. J. M. (2000) · Biochemical Journal · doi:10.1042/bj3500547 · Cited by 30

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
DOI: 10.1046/j.1365-201x.1997.00222.x
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
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor, 2192 d)
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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Rate of oxidative phosphorylation in isolated mitochondria from human skeletal muscle: effect of training status

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