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 demonstration of impaired OXPHOS capacity at relatively low ex vivo flux rates emphasizes the potential importance of the finding, since in vivo flux rates are higher.
“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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“Isolation of Mitochondria Muscle tissue was immediately weighed and added to ice-cold isolation medium followed by the isolation protocol described in detail elsewhere (Tonkonogi and Sahlin, 1997) (Supplemental Experimental Procedures).”
MethodSelf-citationMitochondrial respiration is decreased in skeletal muscle of patients with type 2 diabetes
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“The low E. Gnaiger / The International Journal of Biochemistry & Cell Biology 41 (2009) 1837–1845 1843 mitochondrial activities in a comparable approach with isolated mitochondria (Tonkonogi and Sahlin, 1997) cannot be explained on the basis of aerobic fitness levels (Fig.”
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“centrifugation, as previously described by Tonkonogi and Sahlin (48).”
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“Isolation of human skeletal muscle mitochondria was performed as described previously (35, 36).”
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“The TA was immediately processed for mitochondrial isolation, essentially according to Tonkonogi and Sahlin (1997).”
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“On the other hand, in subjects receiving a different intensity of exercise, muscle citrate synthase (CS) activity, a determinant of mitochondrial number (or volume), was closely correlated to VO2max [7,8].”
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“The other portion (72—202 mg) was used for preparation of isolated mitochondria, as previously described (Tonkonogi & Sahlin, 1997).”
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“Another portion was used for preparation of isolated mitochondria according to the method of Tonkonogi & Sahlin (1997).”
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“The major part of the biopsy was used for isolation of mitochondria as described previously [31].”
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“The other portion ( 100 mg) was immediately used for isolation of mitochondria as previously described (42).”
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BackgroundResultSelf-citationTonkonogi, M., Harris, B. A., & Sahlin, K. (1998) · The Journal of Physiology · doi:10.1111/j.1469-7793.1998.279bz.x · Cited by 92 · see citing works
“…and taking muscle free-ADP concentration to be 6·7—20 ìÒ (Radda, 1986; Sahlin et al. 1997) and mitochondrial Km for ADP to be 11—20 ìÒ (Chance & Williams, 1955; Saks et al. 1995; Tonkonogi & Sahlin, 1997), it can be calculated that muscle respiration at rest should be 25—65% of maximal respiration.”
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“Maximal VO2 in skeletal muscle Tonkonogi and Sahlin paid attention to the fact that the maximal VO2 in intact human skeletal muscle is, when recalculated for the amount of mitochondria, 2-5 times greater than the maximal VO2 in isolated mitochondria, skinned fibers and muscle homogenate [47].”
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“This has become possible by increasing the sensitivity of the method by (i) developing a custom-made oxygraph with extraordinarily small measuring chamber, (ii) construction of powerful electronics for amplification of the relatively weak signal, or (iii) optimization of the procedure for isolation of mitochondria (fo…”
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“4, followed by differential centrifugation [40].”
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“The major part of the muscle biopsy was used for mitochondrial isolation as described previously (Tonkonogi & Sahlin, 1997).”
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“Mitochondria were isolated as previously described (Tonkonogi & Sahlin, 1997).”
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“Nevertheless, strong correlation has been observed between VO2max and mitochondrial parameters or oxidative capacities in skinned fibers (Tonkonogi and Sahlin, 1997; Zoll et al., 2002).”
BackgroundResultRegulation of oxidative phosphorylation in different muscles and various experimental conditions
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Self-citationIncreased mitochondrial substrate sensitivity in skeletal muscle of patients with type 2 diabetes.
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“Isolation of mitochondria from skeletal muscle has been described in detail elsewhere [22].”
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“Another portion (average 110 mg) was used to isolate mitochondria as previously described (34).”
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“…this new knowledge into more individualised exercise prescriptions to improve performance and to better prevent and manage diseases strongly linked to physical inactivity. is the activity of citrate synthase (CS), an enzyme exclusively located in the mitochondria (Tonkonogi & Sahlin, 1997).”
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Impact of Lifelong Sedentary Behavior on Mitochondrial Function of Mice Skeletal Muscle
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Figueiredo, P., Ferreira, R. M., Appell, H.-J., & Duarte, J. A. (2008) · The Journals of Gerontology Series A · doi:10.1093/gerona/63.4.350 · Cited by 65 · see citing works
“Skeletal muscle mitochondria were prepared by conventional methods of differential centrifugation, as previously described by Tonkonogi and Sahlin (25).”
MethodOliveira, R. L. G. S., Ueno, M., de Souza, C. T., Pereira-da-Silva, M., Gasparetti, A. L., Bezzera, R. M. N., Alberici, L. C., Vercesi, A. E., Saad, M. J. A., & Velloso, L. A. (2004) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00103.2004 · Cited by 65 · see citing works
“4) followed by differential centrifugation (40).”
Basse, A. L., Agerholm, M., Farup, J., Dalbram, E., Nielsen, J., Ørtenblad, N., Altıntaş, A., Ehrlich, A. M., Krag, T. O. B., Bruzzone, S., et al. (2021) · Molecular Metabolism · doi:10.1016/j.molmet.2021.101271 · Cited by 62 · see citing works
“Mitochondrial swelling assay Mitochondria were isolated from the freshly dissected gastrocnemius muscles of 4- to 5-week-old WT and SMNKO mice, following the procedure described in [36].”
MethodInfluentialEsther Phielix, E., Jeleník, T., Nowotny, P., Szendroedi, J., & Roden, M. (2013) · Diabetologia · doi:10.1007/s00125-013-3127-2 · Cited by 66 · see citing works
“Isolation of mitochondria Muscle tissue (250–300 mg) was used to isolate mitochondria according to a previously described protocol [22].”
MethodBladder cancer-induced skeletal muscle wasting: disclosing the role of mitochondria plasticity.
Padrão, A., Oliveira, P., Vitorino, R., Colaço, B., Pires, M., Márquez, M., Castellanos, E., Neuparth, M., Teixeira, C., Costa, C., et al. (2013) · International Journal of Biochemistry and Cell Biology · doi:10.1016/j.biocel.2013.04.014 · Cited by 61 · see citing works
Mitochondrial gene expression in elite cyclists: effects of high-intensity interval exercise
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“Muscle oxidative power correlates strongly with aerobic training status and endurance performance (Holloszy 1967; Irrcher et al. 2003; Tonkonogi and Sahlin 1997 ).”
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“…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).”
BackgroundResultJarmuszkiewicz, 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 58 · see citing works
Human quadricepts muscle mitochondria: A functional characterization
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“This muscle is known to be very homogenous with about 55% type I oxidative fibres and the content of connective tissue is modest [17].”
BackgroundTonkonogi, M., Krook, A., Walsh, B. J., & Sahlin, K. (2000) · Biochemical Journal · doi:10.1042/bj3510805 · Cited by 58 · see citing works
Self-citationSahlin, 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 54 · see citing works
“The remaining part (100–250 mg) was weighed and used for mitochondrial isolation as described previously (48).”
MethodSelf-citationSodium 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 · see citing works
“increases in Vmax with endurance training (14, 53, 59).”
BackgroundSelf-citationPuente‐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 53 · see citing works
“However, we isolated mitochondria using well established techniques (27, 33), both in patients and in control subjects.”
BackgroundMethodPuntel, 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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
“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).”
BackgroundAMP Deamination Delays Muscle Acidification during Heavy Exercise and Hypoxia
Korzeniewski, B. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m510418200 · Cited by 48 · see citing works
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 · see citing works
“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).”
MethodMogensen, M., & Sahlin, K. (2005) · Acta Physiologica Scandinavica · doi:10.1111/j.1365-201x.2005.01488.x · Cited by 45 · see citing works
“Mitochondria were isolated with a technique previously described in detail (Tonkonogi & Sahlin 1997).”
MethodResultSelf-citationAgerholm, 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 43 · see citing works
Bakkman, L., Sahlin, K., Holmberg, H., & Tonkonogi, M. (2007) · Acta Physiologica · doi:10.1111/j.1748-1716.2007.01683.x · Cited by 44 · see citing works
“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-citationMitochondrial 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 · see citing works
Boushel, R., & Saltin, B. (2012) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2012.09.024 · Cited by 38 · see citing works
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 · see citing works
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 · see citing works
Self-citationEnhanced 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 · see citing works
“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…”
BackgroundLifelong 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 · see citing works
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 · see citing works
“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…”
BackgroundVitamin 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 · see citing works
“Skeletal muscle mitochondria were prepared by conventional methods involving differential centrifugation, as previously described by Tonkonogi and Sahlin [18].”
MethodN’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 · see citing works
“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].”
BackgroundBak, S. Y., León, I. R., Jensen, O. N., & Højlund, K. (2013) · Journal of Proteome Research · doi:10.1021/pr400281r · Cited by 33 · see citing works
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 31 · see citing works
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 · see citing works
“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-citationKorzeniewski, B. (2016) · Progress in Biophysics and Molecular Biology · doi:10.1016/j.pbiomolbio.2016.12.001 · Cited by 31 · see citing works
“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).”
BackgroundInfluentialBroatch, 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 31 · see citing works
“Located exclusively in the mitochondria (65), CS is an enzyme commonly used in exercise-training studies as a biomarker of mitochondrial content (11, 38).”
MethodTamaki, 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 · see citing works
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 27 · see citing works
Roussel, D., Lhenry, F., Ecochard, L., SEMPORE, B., Rouanet, J., & Favier, R. J. M. (2000) · Biochemical Journal · doi:10.1042/bj3500547 · Cited by 30 · see citing works
- 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 › Complementary and alternative medicine › Cardiovascular and exercise physiology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
- Health Sciences › Medicine › Rehabilitation › 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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