Metabolic adaptations in skeletal muscle, adipose tissue, and whole-body oxidative capacity in response to resistance training

European Journal of Applied Physiology

Volumn 114, Issue 7, 2014, Pages 1463-1471

  Alvehus, Malin ^a   Boman, Niklas ^a   Söderlund, Karin ^b   Svensson, Michael B ^a   Burén, Jonas ^a  

^a UMEÅ UNIVERSITY   (Sweden)

^b SWEDISH SCHOOL OF SPORT AND HEALTH SCIENCES   (Sweden)

Author keywords

Adipose tissue; Enzyme activity; Gene expression; Oxidative capacity; Resistance training; Skeletal muscle

Indexed keywords

BIOLOGICAL MARKER;

ADAPTATION; ADIPOSE TISSUE; ADULT; BLOOD; BODY COMPOSITION; ENERGY METABOLISM; GENE EXPRESSION REGULATION; GENETICS; HUMAN; MALE; METABOLISM; MUSCLE MITOCHONDRION; NORMAL HUMAN; OXIDATION REDUCTION REACTION; OXYGEN CONSUMPTION; RESISTANCE TRAINING; SKELETAL MUSCLE; TIME; YOUNG ADULT;

ADAPTATION, PHYSIOLOGICAL; ADIPOSE TISSUE; ADULT; BIOLOGICAL MARKERS; BODY COMPOSITION; ENERGY METABOLISM; GENE EXPRESSION REGULATION; HEALTHY VOLUNTEERS; HUMANS; MALE; MITOCHONDRIA, MUSCLE; MUSCLE, SKELETAL; OXIDATION-REDUCTION; OXYGEN CONSUMPTION; RESISTANCE TRAINING; TIME FACTORS; YOUNG ADULT;

EID: 84902539137     PISSN: 14396319     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00421-014-2879-9     Document Type: Article

References (49)

1. Alp PR, Newsholme EA, Zammit VA (1976) Activities of citrate synthase and NAD+-linked and NADP+-linked isocitrate dehydrogenase in muscle from vertebrates and invertebrates. Biochem J 154:689-700
2. Andersen P, Saltin B (1985) Maximal perfusion of skeletal muscle in man. J Physiol 366:233-249
3. Arany Z (2008) PGC-1 coactivators and skeletal muscle adaptations in health and disease. Curr Opin Genet Dev 18:426-434
4. Bell GJ, Syrotuik D, Martin TP, Burnham R, Quinney HA (2000) Effect of concurrent strength and endurance training on skeletal muscle properties and hormone concentrations in humans. Eur J Appl Physiol 81:418-427
5. Berthon PM, Howlett RA, Heigenhauser GJ, Spriet LL (1998) Human skeletal muscle carnitine palmitoyltransferase I activity determined in isolated intact mitochondria. J Appl Physiol 85:148-153
6. Bluher M, Bullen JW Jr, Lee JH, Kralisch S, Fasshauer M, Kloting N, Niebauer J, Schon MR, Williams CJ, Mantzoros CS (2006) Circulating adiponectin and expression of adiponectin receptors in human skeletal muscle: associations with metabolic parameters and insulin resistance and regulation by physical training. J Clin Endocrinol Metab 91:2310-2316
7. Bluher M, Williams CJ, Kloting N, Hsi A, Ruschke K, Oberbach A, Fasshauer M, Berndt J, Schon MR, Wolk A, Stumvoll M, Mantzoros CS (2007) Gene expression of adiponectin receptors in human visceral and subcutaneous adipose tissue is related to insulin resistance and metabolic parameters and is altered in response to physical training. Diabetes Care 30:3110-3115
8. Burgomaster KA, Cermak NM, Phillips SM, Benton CR, Bonen A, Gibala MJ (2007) Divergent response of metabolite transport proteins in human skeletal muscle after sprint interval training and detraining. Am J Physiol Regul Integr Comp Physiol 292:R1970-R1976
9. Burgomaster KA, Howarth KR, Phillips SM, Rakobowchuk M, Macdonald MJ, McGee SL, Gibala MJ (2008) Similar metabolic adaptations during exercise after low volume sprint interval and traditional endurance training in humans. J Physiol 586:151-160
10. Camera DM, Anderson MJ, Hawley JA, Carey AL (2010) Short-term endurance training does not alter the oxidative capacity of human subcutaneous adipose tissue. Eur J Appl Physiol 109:307-316
11. Chilibeck PD, Syrotuik DG, Bell GJ (1999) The effect of strength training on estimates of mitochondrial density and distribution throughout muscle fibres. Eur J Appl Physiol 80:604-609
12. Christiansen T, Paulsen SK, Bruun JM, Ploug T, Pedersen SB, Richelsen B (2010) Diet-induced weight loss and exercise alone and in combination enhance the expression of adiponectin receptors in adipose tissue and skeletal muscle, but only diet-induced weight loss enhanced circulating adiponectin. J Clin Endocrinol Metab 95:911-919
13. Civitarese AE, Ukropcova B, Carling S, Hulver M, DeFronzo RA, Mandarino L, Ravussin E, Smith SR (2006) Role of adiponectin in human skeletal muscle bioenergetics. Cell Metab 4:75-87
14. Coen PM, Goodpaster BH (2012) Role of intramyocelluar lipids in human health. Trends Endocrinol Metab 23:391-398
15. de Salles BF, Simao R, Fleck SJ, Dias I, Kraemer-Aguiar LG, Bouskela E (2010) Effects of resistance training on cytokines. Int J Sports Med 31:441-450
16. duManoir GR, Haykowsky MJ, Syrotuik DG, Taylor DA, Bell GJ (2007) The effect of high-intensity rowing and combined strength and endurance training on left ventricular systolic function and morphology. Int J Sports Med 28:488-494
17. Essen B, Jansson E, Henriksson J, Taylor AW, Saltin B (1975) Metabolic characteristics of fibre types in human skeletal muscle. Acta Physiol Scand 95:153-165
18. Fruebis J, Tsao TS, Javorschi S, Ebbets-Reed D, Erickson MR, Yen FT, Bihain BE, Lodish HF (2001) Proteolytic cleavage product of 30-kDa adipocyte complement-related protein increases fatty acid oxidation in muscle and causes weight loss in mice. Proc Natl Acad Sci USA 98:2005-2010
19. Green H, Dahly A, Shoemaker K, Goreham C, Bombardier E, Ball-Burnett M (1999a) Serial effects of high-resistance and prolonged endurance training on Na+-K+ pump concentration and enzymatic activities in human vastus lateralis. Acta Physiol Scand 165:177-184
20. Green H, Goreham C, Ouyang J, Ball-Burnett M, Ranney D (1999b) Regulation of fiber size, oxidative potential, and capillarization in human muscle by resistance exercise. Am J Physiol 276:R591-R596
21. Harwood HJ Jr (2012) The adipocyte as an endocrine organ in the regulation of metabolic homeostasis. Neuropharmacology 63:57-75
22. Hoppeler H, Fluck M (2003) Plasticity of skeletal muscle mitochondria: structure and function. Med Sci Sports Exerc 35:95-104
23. Iwabu M, Yamauchi T, Okada-Iwabu M, Sato K, Nakagawa T, Funata M, Yamaguchi M, Namiki S, Nakayama R, Tabata M, Ogata H, Kubota N, Takamoto I, Hayashi YK, Yamauchi N, Waki H, Fukayama M, Nishino I, Tokuyama K, Ueki K, Oike Y, Ishii S, Hirose K, Shimizu T, Touhara K, Kadowaki T (2010) Adiponectin and AdipoR1 regulate PGC-1alpha and mitochondria by Ca(2+) and AMPK/SIRT1. Nature 464:1313-1319
24. Jeppesen J, Kiens B (2012) Regulation and limitations to fatty acid oxidation during exercise. J Physiol 590:1059-1068
25. Jeukendrup AE, Wallis GA (2005) Measurement of substrate oxidation during exercise by means of gas exchange measurements. Int J Sports Med 26(Suppl 1):S28-S37
26. Kang C, Li Ji L (2012) Role of PGC-1alpha signaling in skeletal muscle health and disease. Ann N Y Acad Sci 1271:110-117
27. Larsen S, Nielsen J, Hansen CN, Nielsen LB, Wibrand F, Stride N, Schroder HD, Boushel R, Helge JW, Dela F, Hey-Mogensen M (2012) Biomarkers of mitochondrial content in skeletal muscle of healthy young human subjects. J Physiol 590:3349-3360
28. Luthi JM, Howald H, Claassen H, Rosler K, Vock P, Hoppeler H (1986) Structural changes in skeletal muscle tissue with heavy-resistance exercise. Int J Sports Med 7:123-127
29. Pesta D, Hoppel F, Macek C, Messner H, Faulhaber M, Kobel C, Parson W, Burtscher M, Schocke M, Gnaiger E (2011) Similar qualitative and quantitative changes of mitochondrial respiration following strength and endurance training in normoxia and hypoxia in sedentary humans. Am J Physiol Regul Integr Comp Physiol 301:R1078-R1087
30. Ratamess NA, Alvar BA, Evetoch TK, Housh TJ, Kibler WB, Kraemer WJ, Triplett NT (2009) American college of sports medicine position stand. Progression models in resistance training for healthy adults. Med Sci Sports Exerc 41:687-708
31. Ruas JL, White JP, Rao RR, Kleiner S, Brannan KT, Harrison BC, Greene NP, Wu J, Estall JL, Irving BA, Lanza IR, Rasbach KA, Okutsu M, Nair KS, Yan Z, Leinwand LA, Spiegelman BM (2012) A PGC-1alpha isoform induced by resistance training regulates skeletal muscle hypertrophy. Cell 151:1319-1331
32. Ruschke K, Fishbein L, Dietrich A, Kloting N, Tonjes A, Oberbach A, Fasshauer M, Jenkner J, Schon MR, Stumvoll M, Bluher M, Mantzoros CS (2010) Gene expression of PPARgamma and PGC-1alpha in human omental and subcutaneous adipose tissues is related to insulin resistance markers and mediates beneficial effects of physical training. Eur J Endocrinol 162:515-523
33. Saltin B, Calbet JA (2006) Point: in health and in a normoxic environment, VO2 max is limited primarily by cardiac output and locomotor muscle blood flow. J Appl Physiol (1985) 100:744-745
34. Serra D, Mera P, Malandrino MI, Mir JF, Herrero L (2013) Mitochondrial fatty acid oxidation in obesity. Antioxid Redox Signal 19(3):269-284
35. 2 max and aerobic exercise performance: a systematic review and meta-analysis. Scand J Med Sci Sports 23:e341-e352
36. Steding K, Engblom H, Buhre T, Carlsson M, Mosen H, Wohlfart B, Arheden H (2010) Relation between cardiac dimensions and peak oxygen uptake. J Cardiovasc Magn Reson 12:8
37. Stepto NK, Benziane B, Wadley GD, Chibalin AV, Canny BJ, Eynon N, McConell GK (2012) Short-term intensified cycle training alters acute and chronic responses of PGC1alpha and cytochrome c oxidase IV to exercise in human skeletal muscle. PLoS One 7:e53080
38. Tanaka H, Swensen T (1998) Impact of resistance training on endurance performance. A new form of cross-training? Sports Med 25:191-200
39. Tang JE, Hartman JW, Phillips SM (2006) Increased muscle oxidative potential following resistance training induced fibre hypertrophy in young men. Appl Physiol Nutr Metab 31:495-501
40. Tesch PA, Komi PV, Hakkinen K (1987) Enzymatic adaptations consequent to long-term strength training. Int J Sports Med 8(Suppl 1):66-69
41. Tesch PA, Thorsson A, Colliander EB (1990) Effects of eccentric and concentric resistance training on skeletal muscle substrates, enzyme activities and capillary supply. Acta Physiol Scand 140:575-580
42. Tunstall RJ, Mehan KA, Wadley GD, Collier GR, Bonen A, Hargreaves M, Cameron-Smith D (2002) Exercise training increases lipid metabolism gene expression in human skeletal muscle. Am J Physiol Endocrinol Metab 283:E66-E72
43. Utomi V, Oxborough D, Whyte GP, Somauroo J, Sharma S, Shave R, Atkinson G, George K (2013) Systematic review and meta-analysis of training mode, imaging modality and body size influences on the morphology and function of the male athlete's heart. Heart 99:1727-1733
44. Wang N, Hikida RS, Staron RS, Simoneau JA (1993) Muscle fiber types of women after resistance training-quantitative ultrastructure and enzyme activity. Pflugers Arch 424:494-502
45. Wang L, Mascher H, Psilander N, Blomstrand E, Sahlin K (2011) Resistance exercise enhances the molecular signaling of mitochondrial biogenesis induced by endurance exercise in human skeletal muscle. J Appl Physiol 111:1335-1344
46. Yamauchi T, Kamon J, Minokoshi Y, Ito Y, Waki H, Uchida S, Yamashita S, Noda M, Kita S, Ueki K, Eto K, Akanuma Y, Froguel P, Foufelle F, Ferre P, Carling D, Kimura S, Nagai R, Kahn BB, Kadowaki T (2002) Adiponectin stimulates glucose utilization and fatty-acid oxidation by activating AMP-activated protein kinase. Nat Med 8:1288-1295
47. Yang SY, He XY, Schulz H (2005) 3-Hydroxyacyl-CoA dehydrogenase and short chain 3-hydroxyacyl-CoA dehydrogenase in human health and disease. FEBS J 272:4874-4883
48. Yilmaz DC, Buyukakilli B, Gurgul S, Rencuzogullari I (2013) Adaptation of heart to training: a comparative study using echocardiography & impedance cardiography in male & female athletes. Indian J Med Res 137:1111-1120
49. 2 cost of cycling during moderate-intensity exercise. Eur J Appl Physiol 112:4151-4161