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Int J Sports Med 2014; 35(10): 863-870
DOI: 10.1055/s-0034-1367045
Genetics & Molecular Biology
© Georg Thieme Verlag KG Stuttgart · New York

Futsal and Continuous Exercise Induce Similar Changes in Specific Skeletal Muscle Signalling Proteins

F. R. Serpiello
1   Institute of Sport, Exercise and Active Living (ISEAL), College of Sport and Exercise Science, Victoria University, Melbourne, Australia
,
M. J. McKenna
1   Institute of Sport, Exercise and Active Living (ISEAL), College of Sport and Exercise Science, Victoria University, Melbourne, Australia
,
G. Coratella
2   Department of Neurological, Neuropsychological, Morphological and ­Movement Sciences, Faculty of Sport Sciences, University of Verona, Italy
,
J. F. Markworth
3   The University of Auckland, Liggins Institute, Auckland, New Zealand
,
C. Tarperi
2   Department of Neurological, Neuropsychological, Morphological and ­Movement Sciences, Faculty of Sport Sciences, University of Verona, Italy
,
D. Bishop
1   Institute of Sport, Exercise and Active Living (ISEAL), College of Sport and Exercise Science, Victoria University, Melbourne, Australia
,
N. K. Stepto
1   Institute of Sport, Exercise and Active Living (ISEAL), College of Sport and Exercise Science, Victoria University, Melbourne, Australia
,
D. Cameron-Smith
3   The University of Auckland, Liggins Institute, Auckland, New Zealand
,
F. Schena
2   Department of Neurological, Neuropsychological, Morphological and ­Movement Sciences, Faculty of Sport Sciences, University of Verona, Italy
› Author Affiliations
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Publication History



accepted after revision 19 December 2013

Publication Date:
27 February 2014 (online)

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Abstract

Exercise elicits skeletal-muscle adaptations which are important for improved health outcomes. We compared the effects of a futsal game (FUT) and moderate-intensity continuous exercise (MOD), on the skeletal-muscle protein signalling responses in young, healthy individuals. 16 men undertook an incremental exercise test and a resting muscle biopsy performed >48 h apart. They were then randomly allocated to either FUT (n=12) consisting of 2 x 20 min halves, or MOD (n=8) consisting of a work-matched running bout performed at an intensity corresponding to the individual ventilatory threshold 1. Work matching was achieved by means of triaxial accelerometers. Immediately after FUT and MOD, participants underwent a second biopsy to assess exercise-induced changes in protein signalling. Total and phosphorylated protein abundance was assessed via western blotting. Both FUT and MOD altered signalling responses in skeletal muscle. FUT increased total ATF2 protein abundance (p=0.048) and phosphorylation (p=0.029), while no changes occurred with MOD. Both exercise regimes increased ACC phosphorylation (p=0.01) and returned a trend for increased p38MAPK phosphorylation. Futsal may be employed as an alternative to continuous exercise to elicit muscle adaptations which may be associated with improved health outcomes. As only FUT increased ATF2 activation, this protein might be a target of future investigation on exercise-induced signalling.

Key words

intermittent exercise - protein signalling - ATF2 - football
 

  • References

  • 1 Akimoto T, Pohnert SC, Li P, Zhang M, Gumbs C, Rosenberg PB, Williams RS, Yan Z. Exercise stimulates Pgc-1alpha transcription in skeletal muscle through activation of the p38 MAPK pathway. J Biol Chem 2005; 280: 19587-19593
    CrossrefPubMedGoogle Scholar
  • 2 Aydin J, Korhonen T, Tavi P, Allen DG, Westerblad H, Bruton JD. Activation of Ca(2+)-dependent protein kinase II during repeated contractions in single muscle fibres from mouse is dependent on the frequency of sarcoplasmic reticulum Ca(2+) release. Acta Physiol (Oxf) 2007; 191: 131-137
    CrossrefPubMedGoogle Scholar
  • 3 Barbero-Alvarez JC, Soto VM, Barbero-Alvarez V, Granda-Vera J. Match analysis and heart rate of futsal players during competition. J Sports Sci 2008; 26: 63-73
    CrossrefPubMedGoogle Scholar
  • 4 Bartlett JD, Hwa Joo C, Jeong TS, Louhelainen J, Cochran AJ, Gibala MJ, Gregson W, Close GL, Drust B, Morton JP. Matched work high-intensity interval and continuous running induce similar increases in PGC-1alpha mRNA, AMPK, p38, and p53 phosphorylation in human skeletal muscle. J Appl Physiol 2012; 112: 1135-1143
    CrossrefPubMedGoogle Scholar
  • 5 Benziane B, Burton TJ, Scanlan B, Galuska D, Canny BJ, Chibalin AV, Zierath JR, Stepto NK. Divergent cell signaling after short-term intensified endurance training in human skeletal muscle. Am J Physiol 2008; 295: E1427-E1438
    CrossrefPubMedGoogle Scholar
  • 6 Bhoumik A, Lopez-Bergami P, Ronai Z. ATF2 on the double-activating transcription factor and DNA damage response protein. Pigment Cell Res 2007; 20: 498-506
    CrossrefPubMedGoogle Scholar
  • 7 Boyd LJ, Ball K, Aughey RJ. The reliability of MinimaxX accelerometers for measuring physical activity in Australian football. Int J Sports Physiol Perform 2011; 6: 311-321
    PubMedGoogle Scholar
  • 8 Caiozzo VJ, Davis JA, Ellis JF, Azus JL, Vandagriff R, Prietto CA, McMaster WC. A comparison of gas exchange indices used to detect the anaerobic threshold. J Appl Physiol 1982; 53: 1184-1189
    PubMedGoogle Scholar
  • 9 Castagna C, D’Ottavio S, Granda Vera J, Barbero Alvarez JC. Match demands of professional Futsal: a case study. J Sci Med Sport 2009; 12: 490-494
    CrossrefPubMedGoogle Scholar
  • 10 Chen ZP, Stephens TJ, Murthy S, Canny BJ, Hargreaves M, Witters LA, Kemp BE, McConell GK. Effect of exercise intensity on skeletal muscle AMPK signaling in humans. Diabetes 2003; 52: 2205-2212
    CrossrefPubMedGoogle Scholar
  • 11 Coffey G, Hawley J. The molecular bases of training adaptation. Sports Med 2007; 37: 737-763
    CrossrefPubMedGoogle Scholar
  • 12 Doherty M, Smith P, Hughes M, Davison R. Caffeine lowers perceptual response and increases power output during high-intensity cycling. J Sports Sci 2004; 22: 637-643
    CrossrefPubMedGoogle Scholar
  • 13 Dzamko N, Schertzer JD, Ryall JG, Steel R, Macaulay SL, Wee S, Chen ZP, Michell BJ, Oakhill JS, Watt MJ, Jorgensen SB, Lynch GS, Kemp BE, Steinberg GR. AMPK-independent pathways regulate skeletal muscle fatty acid oxidation. J Physiol 2008; 586: 5819-5831
    CrossrefPubMedGoogle Scholar
  • 14 Egan B, Carson BP, Garcia-Roves PM, Chibalin AV, Sarsfield FM, Barron N, McCaffrey N, Moyna NM, Zierath JR, O’Gorman DJ. Exercise intensity-dependent regulation of peroxisome proliferator-activated receptor coactivator-1 mRNA abundance is associated with differential activation of upstream signalling kinases in human skeletal muscle. J Physiol 2010; 588: 1779-1790
    CrossrefPubMedGoogle Scholar
  • 15 Eriksson KF, Lindgarde F. Prevention of type 2 (non-insulin-dependent) diabetes mellitus by diet and physical exercise. The 6-year Malmo feasibility study. Diabetologia 1991; 34: 891-898
    CrossrefPubMedGoogle Scholar
  • 16 Gibala MJ, Little JP, Essen Mv, Wilkin GP, Burgomaster KA, Safdar A, Raha S, Tarnopolsky A. Short-term sprint interval versus traditional endurance training: similar initial adaptations in human skeletal muscle and exercise performance. J Physiol 2006; 573: 901-911
    PubMedGoogle Scholar
  • 17 Harriss DJ, Atkinson G. Ethical standards in sport and exercise science research: 2014 update. Int J Sports Med 2013; 34: 1025-1028
    Article in Thieme ConnectPubMedGoogle Scholar
  • 18 Hendrick P, Boyd T, Low O, Takarangi K, Paterson M, Claydon L, Milosavljevic S. Construct validity of RT3 accelerometer: a comparison of level-ground and treadmill walking at self-selected speeds. J Rehabil Res Dev 2010; 47: 157-168
    CrossrefPubMedGoogle Scholar
  • 19 Hopkins W A spreadsheet for analysis of straightforward controlled trials. Sportscience 7, sportsci.org/jour/03/wghtrials.htm. 2003 (Access Date 24-12-2011)
    PubMed
  • 20 Jager S, Handschin C, St-Pierre J, Spiegelman BM. AMP-activated protein kinase (AMPK) action in skeletal muscle via direct phosphorylation of PGC-1alpha. Proc Natl Acad Sci USA 2007; 104: 12017-12022
    CrossrefPubMedGoogle Scholar
  • 21 Jakobsen SN, Hardie DG, Morrice N, Tornqvist HE. 5'-AMP-activated protein kinase phosphorylates IRS-1 on Ser-789 in mouse C2C12 myotubes in response to 5-aminoimidazole-4-carboxamide riboside. J Biol Chem 2001; 276: 46912-46916
    CrossrefPubMedGoogle Scholar
  • 22 Kiens B. Skeletal muscle lipid metabolism in exercise and insulin resistance. Physiol Rev 2006; 86: 205-243
    CrossrefPubMedGoogle Scholar
  • 23 Krustrup P, Nielsen JJ, Krustrup BR, Christensen JF, Pedersen H, Randers MB, Aagaard P, Petersen AM, Nybo L, Bangsbo J. Recreational soccer is an effective health-promoting activity for untrained men. Br J Sports Med 2009; 43: 825-831
    CrossrefPubMedGoogle Scholar
  • 24 Lee-Young RS, Palmer MJ, Linden KC, LePlastrier K, Canny BJ, Hargreaves M, Wadley GD, Kemp BE, McConell GK. Carbohydrate ingestion does not alter skeletal muscle AMPK signaling during exercise in humans. Am J Physiol 2006; 291: E566-E573
    PubMedGoogle Scholar
  • 25 Lee SH, Bahn JH, Whitlock NC, Baek SJ. Activating transcription factor 2 (ATF2) controls tolfenamic acid-induced ATF3 expression via MAP kinase pathways. Oncogene 2010; 29: 5182-5192
    CrossrefPubMedGoogle Scholar
  • 26 Lindstrom J, Louheranta A, Mannelin M, Rastas M, Salminen V, Eriksson J, Uusitupa M, Tuomilehto J. The Finnish Diabetes Prevention Study (DPS): Lifestyle intervention and 3-year results on diet and physical activity. Diabetes Care 2003; 26: 3230-3236
    CrossrefPubMedGoogle Scholar
  • 27 Little JP, Safdar A, Bishop D, Tarnopolsky MA, Gibala MJ. An acute bout of high-intensity interval training increases the nuclear abundance of PGC-1alpha and activates mitochondrial biogenesis in human skeletal muscle. Am J Physiol 2011; 300: R1303-R1310
    PubMedGoogle Scholar
  • 28 Liu Z, Cao W. p38 mitogen-activated protein kinase: a critical node linking insulin resistance and cardiovascular diseases in type 2 diabetes mellitus. Endocr Metab Immune Disord Drug Targets 2009; 9: 38-46
    Google Scholar
  • 29 Markworth JF, Cameron-Smith D. Prostaglandin F2α stimulates PI3K/ERK/mTOR signaling and skeletal myotube hypertrophy. Am J Physiol 2011; 300: C671-C682
    CrossrefPubMedGoogle Scholar
  • 30 McGee SL, Hargreaves M. Exercise and myocyte enhancer factor 2 regulation in human skeletal muscle. Diabetes 2004; 53: 1208-1214
    CrossrefPubMedGoogle Scholar
  • 31 McGee SL, Hargreaves M. Histone modifications and exercise adaptations. J Appl Physiol 2011; 110: 258-263
    CrossrefPubMedGoogle Scholar
  • 32 Montessuit C, Rosenblatt-Velin N, Papageorgiou I, Campos L, Pellieux C, Palma T, Lerch R. Regulation of glucose transporter expression in cardiac myocytes: p38 MAPK is a strong inducer of GLUT4. Cardiovasc Res 2004; 64: 94-104
    CrossrefPubMedGoogle Scholar
  • 33 Mukwevho E, Kohn TA, Lang D, Nyatia E, Smith J, Ojuka EO. Caffeine induces hyperacetylation of histones at the MEF2 site on the Glut4 promoter and increases MEF2A binding to the site via a CaMK-dependent mechanism. Am J Physiol 2008; 294: E582-E588
    PubMedGoogle Scholar
  • 34 Rodrigues VM, Ramos GP, Mendes TT, Cabido CE, Melo ES, Condessa LA, Coelho DB, Garcia ES. Intensity of official Futsal matches. J Strength Cond Res 2011; 25: 2482-2487
    CrossrefPubMedGoogle Scholar
  • 35 Roepstorff C, Halberg N, Hillig T, Saha AK, Ruderman NB, Wojtaszewski JF, Richter EA, Kiens B. Malonyl-CoA and carnitine in regulation of fat oxidation in human skeletal muscle during exercise. Am J Physiol 2005; 288: E133-E142
    PubMedGoogle Scholar
  • 36 Rose AJ, Hargreaves M. Exercise increases Ca2+-calmodulin-dependent protein kinase II activity in human skeletal muscle. J Physiol 2003; 533: 303-309
    PubMedGoogle Scholar
  • 37 Rose AJ, Kiens B, Richter EA. Ca2+-calmodulin-dependent protein kinase expression and signalling in skeletal muscle during exercise. J Physiol 2006; 574: 889-903
    CrossrefPubMedGoogle Scholar
  • 38 Serpiello FR, McKenna MJ, Bishop DJ, Aughey RJ, Caldow MK, Cameron-Smith D, Stepto NK. Repeated Sprints Alter Signalling Related to Mitochondrial Biogenesis in Humans. Med Sci Sports Exerc 2012; 44: 827-834
    CrossrefPubMedGoogle Scholar
  • 39 Shaw K, Gennat H, O’Rourke P, Del Mar C. Exercise for overweight or obesity. Cochrane Database Syst Rev 2006; CD003817
    PubMedGoogle Scholar
  • 40 Stepto NK, Benziane B, Wadley GD, Chibalin AV, Canny BJ, Eynon N, McConell GK. 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 2012; 7: e53080
    CrossrefPubMedGoogle Scholar
  • 41 Tessitore A, Meeusen R, Pagano R, Benvenuti C, Tiberi M, Capranica L. Effectiveness of active versus passive recovery strategies after futsal games. J Strength Cond Res 2008; 22: 1402-1412
    CrossrefPubMedGoogle Scholar
  • 42 Thomas DE, Elliott EJ, Naughton GA. Exercise for type 2 diabetes mellitus. Cochrane Database Syst Rev 2006; 3 CD002968
    PubMedGoogle Scholar
  • 43 Tjønna AE, Lee SJ, Rognmo Ø, Stølen TO, Bye A, Haram PM, Loennechen JP, Al-Share QY, Skogvoll E, Slørdahl SA, Kemi OJ, Najjar SM, Wisløff U. Aerobic interval training versus continuous moderate exercise as a treatment for the metabolic syndrome: a pilot study. Circulation 2008; 118: 346-354
    CrossrefPubMedGoogle Scholar
  • 44 Wadley GD, Lee-Young RS, Canny BJ, Wasuntarawat C, Chen ZP, Hargreaves M, Kemp BE, McConell GK. Effect of exercise intensity and hypoxia on skeletal muscle AMPK signaling and substrate metabolism in humans. Am J Physiol 2006; 290: E694-E702
    PubMedGoogle Scholar
  • 45 Westerblad H, Duty S, Allen DG. Intracellular calcium concentration during low-frequency fatigue in isolated single fibers of mouse skeletal muscle. J Appl Physiol 1993; 75: 382-388
    PubMedGoogle Scholar
  • 46 Wu H, Kanatous SB, Thurmond FA, Gallardo T, Isotani E, Bassel-Duby R, Williams RS. Regulation of mitochondrial biogenesis in skeletal muscle by CaMK. Science 2002; 296: 349-352
    CrossrefPubMedGoogle Scholar