Skip to main content
Top
Published in: European Journal of Applied Physiology 1/2016

01-01-2016 | Original Article

Effect of regional muscle location but not adiposity on mitochondrial biogenesis-regulating proteins

Authors: Jesús Gustavo Ponce-González, Ignacio Ara, Steen Larsen, Borja Guerra, Jose A. L. Calbet, Jørn Wulff Helge

Published in: European Journal of Applied Physiology | Issue 1/2016

Login to get access

Abstract

Purpose

The aim of this study was to determine if the expression of the mitochondrial biogenesis-regulating proteins SIRT1, SIRT3 and PGC-1alpha in human skeletal muscle is influenced by adiposity.

Method

Twenty-nine male subjects were recruited into three groups: control (n = 10), obese (n = 10) and post-obese (n = 9). Intentionally, groups were matched by age, aerobic capacity and in addition the control and post-obese groups also by BMI. Muscle biopsies were obtained from the m. deltoid and vastus lateralis. PGC-1alpha, SIRT1 and SIRT3 protein expression was analyzed by Western blot.

Result

PGC-1alpha, SIRT1 and SIRT3 protein expression was similar regardless of the level of adiposity. Only a main effect of group on SIRT1 protein showed a trend toward higher expression in post-obese than control and obese (P = 0.09). Despite similar muscle fiber-type composition (previously reported), PGC-1alpha, SIRT1 and SIRT3 protein expression was higher in leg compared to arm muscle in all groups (P < 0.05).

Conclusion

This study shows that PGC-1alpha, SIRT1 and SIRT3 protein expression in basal conditions was not altered in humans with different levels of adiposity but similar aerobic capacity. The expression of PGC-1alpha, SIRT1 and SIRT3 was higher in vastus lateralis than in deltoid muscle, indicating that local rather than systemic factors prevail in regulating the level of expression of these proteins.
Literature
go back to reference Achten J, Gleeson M, Jeukendrup AE (2002) Determination of the exercise intensity that elicits maximal fat oxidation. Med Sci Sports Exerc 34(1):92–97PubMedCrossRef Achten J, Gleeson M, Jeukendrup AE (2002) Determination of the exercise intensity that elicits maximal fat oxidation. Med Sci Sports Exerc 34(1):92–97PubMedCrossRef
go back to reference Ahlborg G, Jensen-Urstad M (1991) Metabolism in exercising arm vs. leg muscle. Clin Physiol 11(5):459–468PubMedCrossRef Ahlborg G, Jensen-Urstad M (1991) Metabolism in exercising arm vs. leg muscle. Clin Physiol 11(5):459–468PubMedCrossRef
go back to reference Amat R, Planavila A, Chen SL, Iglesias R, Giralt M, Villarroya F (2009) SIRT1 controls the transcription of the peroxisome proliferator-activated receptor-gamma Co-activator-1alpha (PGC-1alpha) gene in skeletal muscle through the PGC-1alpha autoregulatory loop and interaction with MyoD. J Biol Chem 284(33):21872–21880. doi:10.1074/jbc.M109.022749 PubMedPubMedCentralCrossRef Amat R, Planavila A, Chen SL, Iglesias R, Giralt M, Villarroya F (2009) SIRT1 controls the transcription of the peroxisome proliferator-activated receptor-gamma Co-activator-1alpha (PGC-1alpha) gene in skeletal muscle through the PGC-1alpha autoregulatory loop and interaction with MyoD. J Biol Chem 284(33):21872–21880. doi:10.​1074/​jbc.​M109.​022749 PubMedPubMedCentralCrossRef
go back to reference Ara I, Larsen S, Stallknecht B, Guerra B, Morales-Alamo D, Andersen JL, Ponce-Gonzalez JG, Guadalupe-Grau A, Galbo H, Calbet JA, Helge JW (2011) Normal mitochondrial function and increased fat oxidation capacity in leg and arm muscles in obese humans. Int J Obes (Lond) 35(1):99–108. doi:10.1038/ijo.2010.123 CrossRef Ara I, Larsen S, Stallknecht B, Guerra B, Morales-Alamo D, Andersen JL, Ponce-Gonzalez JG, Guadalupe-Grau A, Galbo H, Calbet JA, Helge JW (2011) Normal mitochondrial function and increased fat oxidation capacity in leg and arm muscles in obese humans. Int J Obes (Lond) 35(1):99–108. doi:10.​1038/​ijo.​2010.​123 CrossRef
go back to reference Boushel R, Ara I, Gnaiger E, Helge JW, Gonzalez-Alonso J, Munck-Andersen T, Sondergaard H, Damsgaard R, van Hall G, Saltin B, Calbet JA (2014) Low-intensity training increases peak arm VO2 by enhancing both convective and diffusive O2 delivery. Acta Physiol (Oxf) 211(1):122–134. doi:10.1111/apha.12258 CrossRef Boushel R, Ara I, Gnaiger E, Helge JW, Gonzalez-Alonso J, Munck-Andersen T, Sondergaard H, Damsgaard R, van Hall G, Saltin B, Calbet JA (2014) Low-intensity training increases peak arm VO2 by enhancing both convective and diffusive O2 delivery. Acta Physiol (Oxf) 211(1):122–134. doi:10.​1111/​apha.​12258 CrossRef
go back to reference Chanseaume E, Barquissau V, Salles J, Aucouturier J, Patrac V, Giraudet C, Gryson C, Duche P, Boirie Y, Chardigny JM, Morio B (2010) Muscle mitochondrial oxidative phosphorylation activity, but not content, is altered with abdominal obesity in sedentary men: synergism with changes in insulin sensitivity. J Clin Endocrinol Metab 95(6):2948–2956. doi:10.1210/jc.2009-1938 PubMedCrossRef Chanseaume E, Barquissau V, Salles J, Aucouturier J, Patrac V, Giraudet C, Gryson C, Duche P, Boirie Y, Chardigny JM, Morio B (2010) Muscle mitochondrial oxidative phosphorylation activity, but not content, is altered with abdominal obesity in sedentary men: synergism with changes in insulin sensitivity. J Clin Endocrinol Metab 95(6):2948–2956. doi:10.​1210/​jc.​2009-1938 PubMedCrossRef
go back to reference Chomentowski P, Dube JJ, Amati F, Stefanovic-Racic M, Zhu S, Toledo FG, Goodpaster BH (2009) Moderate exercise attenuates the loss of skeletal muscle mass that occurs with intentional caloric restriction-induced weight loss in older, overweight to obese adults. J Gerontol A Biol Sci Med Sci 64(5):575–580. doi:10.1093/gerona/glp007 PubMedCrossRef Chomentowski P, Dube JJ, Amati F, Stefanovic-Racic M, Zhu S, Toledo FG, Goodpaster BH (2009) Moderate exercise attenuates the loss of skeletal muscle mass that occurs with intentional caloric restriction-induced weight loss in older, overweight to obese adults. J Gerontol A Biol Sci Med Sci 64(5):575–580. doi:10.​1093/​gerona/​glp007 PubMedCrossRef
go back to reference De Filippis E, Alvarez G, Berria R, Cusi K, Everman S, Meyer C, Mandarino LJ (2008) Insulin-resistant muscle is exercise resistant: evidence for reduced response of nuclear-encoded mitochondrial genes to exercise. Am J Physiol Endocrinol Metab 294(3):E607–E614. doi:10.1152/ajpendo.00729.2007 PubMedCrossRef De Filippis E, Alvarez G, Berria R, Cusi K, Everman S, Meyer C, Mandarino LJ (2008) Insulin-resistant muscle is exercise resistant: evidence for reduced response of nuclear-encoded mitochondrial genes to exercise. Am J Physiol Endocrinol Metab 294(3):E607–E614. doi:10.​1152/​ajpendo.​00729.​2007 PubMedCrossRef
go back to reference Fuentes T, Ara I, Guadalupe-Grau A, Larsen S, Stallknecht B, Olmedillas H, Santana A, Helge JW, Calbet JA, Guerra B (2010) Leptin receptor 170 kDa (OB-R170) protein expression is reduced in obese human skeletal muscle: a potential mechanism of leptin resistance. Exp Physiol 95(1):160–171. doi:10.1113/expphysiol.2009.049270 PubMedCrossRef Fuentes T, Ara I, Guadalupe-Grau A, Larsen S, Stallknecht B, Olmedillas H, Santana A, Helge JW, Calbet JA, Guerra B (2010) Leptin receptor 170 kDa (OB-R170) protein expression is reduced in obese human skeletal muscle: a potential mechanism of leptin resistance. Exp Physiol 95(1):160–171. doi:10.​1113/​expphysiol.​2009.​049270 PubMedCrossRef
go back to reference Garcia-Martinez C, Sibille B, Solanes G, Darimont C, Mace K, Villarroya F, Gomez-Foix AM (2001) Overexpression of UCP3 in cultured human muscle lowers mitochondrial membrane potential, raises ATP/ADP ratio, and favors fatty acid vs. glucose oxidation. FASEB J 15(11):2033–2035. doi:10.1096/fj.00-0828fje PubMed Garcia-Martinez C, Sibille B, Solanes G, Darimont C, Mace K, Villarroya F, Gomez-Foix AM (2001) Overexpression of UCP3 in cultured human muscle lowers mitochondrial membrane potential, raises ATP/ADP ratio, and favors fatty acid vs. glucose oxidation. FASEB J 15(11):2033–2035. doi:10.​1096/​fj.​00-0828fje PubMed
go back to reference Gerhart-Hines Z, Rodgers JT, Bare O, Lerin C, Kim SH, Mostoslavsky R, Alt FW, Wu Z, Puigserver P (2007) Metabolic control of muscle mitochondrial function and fatty acid oxidation through SIRT1/PGC-1alpha. EMBO J 26(7):1913–1923PubMedPubMedCentralCrossRef Gerhart-Hines Z, Rodgers JT, Bare O, Lerin C, Kim SH, Mostoslavsky R, Alt FW, Wu Z, Puigserver P (2007) Metabolic control of muscle mitochondrial function and fatty acid oxidation through SIRT1/PGC-1alpha. EMBO J 26(7):1913–1923PubMedPubMedCentralCrossRef
go back to reference Gong DW, Monemdjou S, Gavrilova O, Leon LR, Marcus-Samuels B, Chou CJ, Everett C, Kozak LP, Li C, Deng C, Harper ME, Reitman ML (2000) Lack of obesity and normal response to fasting and thyroid hormone in mice lacking uncoupling protein-3. J Biol Chem 275(21):16251–16257. doi:10.1074/jbc.M910177199 PubMedCrossRef Gong DW, Monemdjou S, Gavrilova O, Leon LR, Marcus-Samuels B, Chou CJ, Everett C, Kozak LP, Li C, Deng C, Harper ME, Reitman ML (2000) Lack of obesity and normal response to fasting and thyroid hormone in mice lacking uncoupling protein-3. J Biol Chem 275(21):16251–16257. doi:10.​1074/​jbc.​M910177199 PubMedCrossRef
go back to reference Guadalupe-Grau A, Rodríguez-García L, Torres-Peralta R, Morales-Álamo D, Ponce-Gonzalez JG, Suarez-Pérez I, Santana A, Calbet JAL (2015) Greater basal skeletal muscle AMPKα phosphorylation in men than in women: Associations with anaerobic performance. Eur J Sport Sci. doi:10.1080/17461391.2015.1063701 PubMed Guadalupe-Grau A, Rodríguez-García L, Torres-Peralta R, Morales-Álamo D, Ponce-Gonzalez JG, Suarez-Pérez I, Santana A, Calbet JAL (2015) Greater basal skeletal muscle AMPKα phosphorylation in men than in women: Associations with anaerobic performance. Eur J Sport Sci. doi:10.​1080/​17461391.​2015.​1063701 PubMed
go back to reference Guerra B, Guadalupe-Grau A, Fuentes T, Ponce-Gonzalez JG, Morales-Alamo D, Olmedillas H, Guillen-Salgado J, Santana A, Calbet JA (2010) SIRT1, AMP-activated protein kinase phosphorylation and downstream kinases in response to a single bout of sprint exercise: influence of glucose ingestion. Eur J Appl Physiol 109(4):731–743. doi:10.1007/s00421-010-1413-y PubMedCrossRef Guerra B, Guadalupe-Grau A, Fuentes T, Ponce-Gonzalez JG, Morales-Alamo D, Olmedillas H, Guillen-Salgado J, Santana A, Calbet JA (2010) SIRT1, AMP-activated protein kinase phosphorylation and downstream kinases in response to a single bout of sprint exercise: influence of glucose ingestion. Eur J Appl Physiol 109(4):731–743. doi:10.​1007/​s00421-010-1413-y PubMedCrossRef
go back to reference Gurd BJ (2011) Deacetylation of PGC-1alpha by SIRT1: importance for skeletal muscle function and exercise-induced mitochondrial biogenesis. Appl Physiol Nutr Metab 36(5):589–597. doi:10.1139/h11-070 PubMedCrossRef Gurd BJ (2011) Deacetylation of PGC-1alpha by SIRT1: importance for skeletal muscle function and exercise-induced mitochondrial biogenesis. Appl Physiol Nutr Metab 36(5):589–597. doi:10.​1139/​h11-070 PubMedCrossRef
go back to reference Gurd BJ, Holloway GP, Yoshida Y, Bonen A (2011) In mammalian muscle, SIRT3 is present in mitochondria and not in the nucleus; and SIRT3 is upregulated by chronic muscle contraction in an adenosine monophosphate-activated protein kinase-independent manner. Metabolism. doi:10.1016/j.metabol.2011.09.016 PubMed Gurd BJ, Holloway GP, Yoshida Y, Bonen A (2011) In mammalian muscle, SIRT3 is present in mitochondria and not in the nucleus; and SIRT3 is upregulated by chronic muscle contraction in an adenosine monophosphate-activated protein kinase-independent manner. Metabolism. doi:10.​1016/​j.​metabol.​2011.​09.​016 PubMed
go back to reference Hirschey MD, Shimazu T, Goetzman E, Jing E, Schwer B, Lombard DB, Grueter CA, Harris C, Biddinger S, Ilkayeva OR, Stevens RD, Li Y, Saha AK, Ruderman NB, Bain JR, Newgard CB, Farese RV Jr, Alt FW, Kahn CR, Verdin E (2010) SIRT3 regulates mitochondrial fatty-acid oxidation by reversible enzyme deacetylation. Nature 464(7285):121–125. doi:10.1038/nature08778 PubMedPubMedCentralCrossRef Hirschey MD, Shimazu T, Goetzman E, Jing E, Schwer B, Lombard DB, Grueter CA, Harris C, Biddinger S, Ilkayeva OR, Stevens RD, Li Y, Saha AK, Ruderman NB, Bain JR, Newgard CB, Farese RV Jr, Alt FW, Kahn CR, Verdin E (2010) SIRT3 regulates mitochondrial fatty-acid oxidation by reversible enzyme deacetylation. Nature 464(7285):121–125. doi:10.​1038/​nature08778 PubMedPubMedCentralCrossRef
go back to reference Holloway GP, Perry CG, Thrush AB, Heigenhauser GJ, Dyck DJ, Bonen A, Spriet LL (2008) PGC-1alpha’s relationship with skeletal muscle palmitate oxidation is not present with obesity despite maintained PGC-1alpha and PGC-1beta protein. Am J Physiol Endocrinol Metab 294(6):E1060–E1069. doi:10.1152/ajpendo.00726.2007 PubMedCrossRef Holloway GP, Perry CG, Thrush AB, Heigenhauser GJ, Dyck DJ, Bonen A, Spriet LL (2008) PGC-1alpha’s relationship with skeletal muscle palmitate oxidation is not present with obesity despite maintained PGC-1alpha and PGC-1beta protein. Am J Physiol Endocrinol Metab 294(6):E1060–E1069. doi:10.​1152/​ajpendo.​00726.​2007 PubMedCrossRef
go back to reference Horowitz JF, Klein S (2000) Oxidation of nonplasma fatty acids during exercise is increased in women with abdominal obesity. J Appl Physiol 89(6):2276–2282PubMed Horowitz JF, Klein S (2000) Oxidation of nonplasma fatty acids during exercise is increased in women with abdominal obesity. J Appl Physiol 89(6):2276–2282PubMed
go back to reference Jing E, Emanuelli B, Hirschey MD, Boucher J, Lee KY, Lombard D, Verdin EM, Kahn CR (2011) Sirtuin-3 (Sirt3) regulates skeletal muscle metabolism and insulin signaling via altered mitochondrial oxidation and reactive oxygen species production. Proc Natl Acad Sci USA 108(35):14608–14613. doi:10.1073/pnas.1111308108 PubMedPubMedCentralCrossRef Jing E, Emanuelli B, Hirschey MD, Boucher J, Lee KY, Lombard D, Verdin EM, Kahn CR (2011) Sirtuin-3 (Sirt3) regulates skeletal muscle metabolism and insulin signaling via altered mitochondrial oxidation and reactive oxygen species production. Proc Natl Acad Sci USA 108(35):14608–14613. doi:10.​1073/​pnas.​1111308108 PubMedPubMedCentralCrossRef
go back to reference Kern DS, Semmler JG, Enoka RM (2001) Long-term activity in upper- and lower-limb muscles of humans. J Appl Physiol 91(5):2224–2232PubMed Kern DS, Semmler JG, Enoka RM (2001) Long-term activity in upper- and lower-limb muscles of humans. J Appl Physiol 91(5):2224–2232PubMed
go back to reference Larsen S, Ara I, Rabol R, Andersen JL, Boushel R, Dela F, Helge JW (2009) Are substrate use during exercise and mitochondrial respiratory capacity decreased in arm and leg muscle in type 2 diabetes? Diabetologia 52(7):1400–1408. doi:10.1007/s00125-009-1353-4 PubMedCrossRef Larsen S, Ara I, Rabol R, Andersen JL, Boushel R, Dela F, Helge JW (2009) Are substrate use during exercise and mitochondrial respiratory capacity decreased in arm and leg muscle in type 2 diabetes? Diabetologia 52(7):1400–1408. doi:10.​1007/​s00125-009-1353-4 PubMedCrossRef
go back to reference Li L, Muhlfeld C, Niemann B, Pan R, Li R, Hilfiker-Kleiner D, Chen Y, Rohrbach S (2011) Mitochondrial biogenesis and PGC-1alpha deacetylation by chronic treadmill exercise: differential response in cardiac and skeletal muscle. Basic Res Cardiol 106(6):1221–1234. doi:10.1007/s00395-011-0213-9 PubMedCrossRef Li L, Muhlfeld C, Niemann B, Pan R, Li R, Hilfiker-Kleiner D, Chen Y, Rohrbach S (2011) Mitochondrial biogenesis and PGC-1alpha deacetylation by chronic treadmill exercise: differential response in cardiac and skeletal muscle. Basic Res Cardiol 106(6):1221–1234. doi:10.​1007/​s00395-011-0213-9 PubMedCrossRef
go back to reference Lima-Silva AE, Bertuzzi RC, Pires FO, Gagliardi JF, Barros RV, Hammond J, Kiss MA (2010) Relationship between training status and maximal fat oxidation rate. J Sports Sci Med 9(1):31–35PubMedPubMedCentral Lima-Silva AE, Bertuzzi RC, Pires FO, Gagliardi JF, Barros RV, Hammond J, Kiss MA (2010) Relationship between training status and maximal fat oxidation rate. J Sports Sci Med 9(1):31–35PubMedPubMedCentral
go back to reference Lin J, Wu H, Tarr PT, Zhang CY, Wu Z, Boss O, Michael LF, Puigserver P, Isotani E, Olson EN, Lowell BB, Bassel-Duby R, Spiegelman BM (2002) Transcriptional co-activator PGC-1 alpha drives the formation of slow-twitch muscle fibres. Nature 418(6899):797–801. doi:10.1038/nature00904 PubMedCrossRef Lin J, Wu H, Tarr PT, Zhang CY, Wu Z, Boss O, Michael LF, Puigserver P, Isotani E, Olson EN, Lowell BB, Bassel-Duby R, Spiegelman BM (2002) Transcriptional co-activator PGC-1 alpha drives the formation of slow-twitch muscle fibres. Nature 418(6899):797–801. doi:10.​1038/​nature00904 PubMedCrossRef
go back to reference Palacios OM, Carmona JJ, Michan S, Chen KY, Manabe Y, Ward JL 3rd, Goodyear LJ, Tong Q (2009) Diet and exercise signals regulate SIRT3 and activate AMPK and PGC-1alpha in skeletal muscle. Aging (Albany NY) 1(9):771–783 Palacios OM, Carmona JJ, Michan S, Chen KY, Manabe Y, Ward JL 3rd, Goodyear LJ, Tong Q (2009) Diet and exercise signals regulate SIRT3 and activate AMPK and PGC-1alpha in skeletal muscle. Aging (Albany NY) 1(9):771–783
go back to reference Ringholm S, Bienso RS, Kiilerich K, Guadalupe-Grau A, Aachmann-Andersen NJ, Saltin B, Plomgaard P, Lundby C, Wojtaszewski JF, Calbet JA, Pilegaard H (2011) Bed rest reduces metabolic protein content and abolishes exercise-induced mRNA responses in human skeletal muscle. Am J Physiol Endocrinol Metab 301(4):E649–E658. doi:10.1152/ajpendo.00230.2011 PubMedCrossRef Ringholm S, Bienso RS, Kiilerich K, Guadalupe-Grau A, Aachmann-Andersen NJ, Saltin B, Plomgaard P, Lundby C, Wojtaszewski JF, Calbet JA, Pilegaard H (2011) Bed rest reduces metabolic protein content and abolishes exercise-induced mRNA responses in human skeletal muscle. Am J Physiol Endocrinol Metab 301(4):E649–E658. doi:10.​1152/​ajpendo.​00230.​2011 PubMedCrossRef
go back to reference Sandri M, Lin J, Handschin C, Yang W, Arany ZP, Lecker SH, Goldberg AL, Spiegelman BM (2006) PGC-1alpha protects skeletal muscle from atrophy by suppressing FoxO3 action and atrophy-specific gene transcription. Proc Natl Acad Sci USA 103(44):16260–16265. doi:10.1073/pnas.0607795103 PubMedPubMedCentralCrossRef Sandri M, Lin J, Handschin C, Yang W, Arany ZP, Lecker SH, Goldberg AL, Spiegelman BM (2006) PGC-1alpha protects skeletal muscle from atrophy by suppressing FoxO3 action and atrophy-specific gene transcription. Proc Natl Acad Sci USA 103(44):16260–16265. doi:10.​1073/​pnas.​0607795103 PubMedPubMedCentralCrossRef
go back to reference Schutz Y, Tremblay A, Weinsier RL, Nelson KM (1992) Role of fat oxidation in the long-term stabilization of body weight in obese women. Am J Clin Nutr 55(3):670–674PubMed Schutz Y, Tremblay A, Weinsier RL, Nelson KM (1992) Role of fat oxidation in the long-term stabilization of body weight in obese women. Am J Clin Nutr 55(3):670–674PubMed
go back to reference Vidal-Puig AJ, Grujic D, Zhang CY, Hagen T, Boss O, Ido Y, Szczepanik A, Wade J, Mootha V, Cortright R, Muoio DM, Lowell BB (2000) Energy metabolism in uncoupling protein 3 gene knockout mice. J Biol Chem 275(21):16258–16266. doi:10.1074/jbc.M910179199 PubMedCrossRef Vidal-Puig AJ, Grujic D, Zhang CY, Hagen T, Boss O, Ido Y, Szczepanik A, Wade J, Mootha V, Cortright R, Muoio DM, Lowell BB (2000) Energy metabolism in uncoupling protein 3 gene knockout mice. J Biol Chem 275(21):16258–16266. doi:10.​1074/​jbc.​M910179199 PubMedCrossRef
go back to reference Wu Z, Puigserver P, Andersson U, Zhang C, Adelmant G, Mootha V, Troy A, Cinti S, Lowell B, Scarpulla RC, Spiegelman BM (1999) Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell 98(1):115–124. doi:10.1016/S0092-8674(00)80611-X PubMedCrossRef Wu Z, Puigserver P, Andersson U, Zhang C, Adelmant G, Mootha V, Troy A, Cinti S, Lowell B, Scarpulla RC, Spiegelman BM (1999) Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell 98(1):115–124. doi:10.​1016/​S0092-8674(00)80611-X PubMedCrossRef
Metadata
Title
Effect of regional muscle location but not adiposity on mitochondrial biogenesis-regulating proteins
Authors
Jesús Gustavo Ponce-González
Ignacio Ara
Steen Larsen
Borja Guerra
Jose A. L. Calbet
Jørn Wulff Helge
Publication date
01-01-2016
Publisher
Springer Berlin Heidelberg
Published in
European Journal of Applied Physiology / Issue 1/2016
Print ISSN: 1439-6319
Electronic ISSN: 1439-6327
DOI
https://doi.org/10.1007/s00421-015-3232-7

Other articles of this Issue 1/2016

European Journal of Applied Physiology 1/2016 Go to the issue