Int J Sports Med 2013; 34(08): 676-687
DOI: 10.1055/s-0032-1323782
Physiology & Biochemistry
© Georg Thieme Verlag KG Stuttgart · New York

Moderate Exercise Training Induces ROS-Related Adaptations to Skeletal Muscles

P. M. Abruzzo
1   Department of Histology, Embryology, and Applied Biology, University of Bologna, Bologna, Italy
,
F. Esposito
2   Department of Biomedical Sciences for Health, University of Milan, Milan, Italy
,
C. Marchionni
1   Department of Histology, Embryology, and Applied Biology, University of Bologna, Bologna, Italy
,
S. di Tullio
1   Department of Histology, Embryology, and Applied Biology, University of Bologna, Bologna, Italy
,
S. Belia
3   Department of Cell and Environmental Biology, Section of Cell and Molecular Biology, University of Perugia, Perugia, Italy
,
S. Fulle
4   Department of Neuroscience and Imaging, University “G. d’Annunzio” of Chieti-Pescara, Chieti, Italy
5   Ce.S.I. – Center for Excellence on Ageing G. d’Annunzio Foundation, Chieti, Italy
6   IIM-Interuniversity Institute of Myology, Italy
,
A. Veicsteinas
2   Department of Biomedical Sciences for Health, University of Milan, Milan, Italy
7   Center of Sport Medicine, Don Gnocchi Foundation, Milan, Italy
,
M. Marini
1   Department of Histology, Embryology, and Applied Biology, University of Bologna, Bologna, Italy
6   IIM-Interuniversity Institute of Myology, Italy
› Author Affiliations
Further Information

Publication History



accepted after revision 15 August 2012

Publication Date:
16 January 2013 (online)

Abstract

Aim of the present work was the evaluation of the effects of moderate exercise training on 2 skeletal muscles differing in fibre-type composition, Tibialis Anterior (TA) and Soleus (SOL). Fibre adaptations, including their metabolic shift and mechanisms underlying proliferation and differentiation, oxidative stress markers, antioxidant and cytoprotective molecules, activity of Ca2+-handling molecules were examined. 6 male 2-month-old rats trained on a treadmill for 1 h/day, 3 days/week, for 14 weeks, reaching 30 m/min at the end of training. 6 age-matched sedentary rats served as controls. Rats were sacrificed 24 h after the last training session. Muscle regulatory factors increased in both muscles, activating satellite cell proliferation, which led to moderate hypertrophy in SOL and to moderate hyperplasia in TA, where the upregulation of desmin and TNFR2 expression suggests that myotube formation by proliferating myoblasts is somehow delayed. Changes leading to a more oxidative metabolism together with the upregulation of a number of antioxidant enzymes occurred in TA. HSP70i protein was upregulated in both SOL and TA, while oxidative stress markers increased in SOL alone. The status of ionic channels and pumps was preserved. We suggest that the increase in ROS, known to be associated with exercise, underlies most observed results.

 
  • References

  • 1 Abruzzo PM, di Tullio S, Marchionni C, Belia S, Fanò G, Zampieri S, Carraro U, Kern H, Sgarbi G, Lenaz G, Marini M. Oxidative stress in denervated rat muscle. Free Rad Res 2010; 44: 563-576
  • 2 Aoi W, Naito Y, Takanami Y, Kawai Y, Sakuma K, Ichikawa H, Yoshida N, Yoshikawa T. Oxidative stress and delayed-onset muscle damage after exercise. Free Rad Biol Med 2004; 37: 480-487
  • 3 Beccafico S, Puglielli C, Pietrangelo T, Bellomo R, Fanò G, Fulle S. Age-dependent effects of functional aspects in human satellite cells. Ann NY Acad Sci 2007; 1100: 345-352
  • 4 Camera DM, Edge J, Short MJ, Hawley JA, Coffey VG. Early time course of Akt phosphorylation following endurance and resistance exercise. Med Sci Sports Exerc 2010; 42: 1843-1852
  • 5 Canepari M, Pellegrino MA, D’Antona G, Bottinelli R. Skeletal muscle fibre diversity and the underlying mechanisms. Acta Physiol (Oxf) 2010; 199: 465-476
  • 6 Charo IF, Ransohoff RM. The many roles of chemokines and chemokine receptors in inflammation. N Engl J Med 2006; 354: 610-621
  • 7 Chen X. Cyclin G: a regulator of the p53-Mdm2 network. Dev Cell 2002; 2: 518-519
  • 8 Chinsomboon J, Ruas J, Gupta RK, Thom R, Shoag J, Rowe GC, Sawada N, Raghuram S, Arany Z. The transcriptional coactivator PGC-1 mediates exercise-induced angiogenesis in skeletal muscle. Proc Natl Acad Sci USA 2009; 106: 21401-21406
  • 9 Conboy IM, Rando TA. The regulation of Notch signaling controls satellite cell activation and cell fate in postnatal myogenesis. Dev Cell 2002; 3: 397-409
  • 10 Egginton S. Invited review: activity-induced angiogenesis. Pflugers Arch 2009; 457: 963-977
  • 11 Esposito F, Ronchi R, Milano G, Margonato V, di Tullio S, Marini M, Veicsteinas A, Samaja M. Myocardial tolerance to ischemia-reperfusion injury, training intensity and cessation. Eur J Appl Physiol 2011; 111: 859-868
  • 12 Flück M, Hoppeler H. Molecular basis of skeletal muscle plasticity – from gene to form and function. Rev Physiol Biochem Pharmacol 2003; 146: 159-216
  • 13 Flück M. Functional, structural and molecular plasticity of mammalian skeletal muscle in response to exercise stimuli. J Exp Biol 2006; 209: 2239-2248
  • 14 Flueck M. Tuning of mitochondrial pathways by muscle work: from triggers to sensors and expression signatures. Appl Physiol Nutr Metab 2009; 34: 447-453
  • 15 Fulle S, Mecocci P, Fanò G, Vecchiet I, Vecchini A, Racciotti D, Cherubini A, Pizzigallo E, Vecchiet L, Senin U, Beal MF. Specific oxidative alterations in vastus lateralis muscle of patients with the diagnosis of chronic fatigue syndrome. Free Rad Biol Med 2000; 29: 1252-1259
  • 16 Fulle S, Belia S, Vecchiet J, Morabito C, Vecchiet L, Fanò G. Modification of the functional capacity of sarcoplasmic reticulum membranes in patients suffering from chronic fatigue syndrome. Neuromuscul Disord 2003; 13: 479-484
  • 17 Harmon BT, Orkunoglu-Suer EF, Adham K, Larkin JS, Gordish-Dressman H, Clarkson PM, Thompson PD, Angelopoulos TJ, Gordon PM, Moyna NM, Pescatello LS, Visich PS, Zoeller RF, Hubal MJ, Tosi LL, Hoffman EP, Devaney JM. CCL2 and CCR2 variants are associated with skeletal muscle strength and change in strength with resistance training. J Appl Physiol 2010; 109: 1779-1785
  • 18 Harriss DJ, Atkinson G. Update – ethical standards in sport and exercise science research. Int J Sports Med 2011; 32: 819-821
  • 19 Horne MC, Goolsby GL, Donaldson KL, Tran D, Neubauer M, Wahl AF. Cyclin G1 and cyclin G2 comprise a new family of cyclins with contrasting tissue-specific and cell cycle-regulated expression. J Biol Chem 1996; 271: 6050-6061
  • 20 Irrcher I, Ljubicic V, Hood DA. Interactions between ROS and AMP kinase activity in the regulation of PGC-1α transcription in skeletal muscle cells. Am J Physiol 2009; 296: C116-C123
  • 21 Jensen MR, Factor VM, Zimonjic DB, Miller M, Keck CL, Thorgeirsson SS. Chromosome localization and structure of the murine cyclin G1 gene promoter sequence. Genomics 1997; 45: 297-303
  • 22 Ji LL, Gomez-Cabrera MC, Vina J. Role of free radicals and antioxidant signaling in skeletal muscle health and pathology. Infect Disord Drug Targets 2009; 9: 428-444
  • 23 Kang C, O’Moore KM, Dickman JR, Ji LL. Exercise activation of muscle peroxisome proliferator-activated receptor-γ coactivator-1α signaling is redox sensitive. Free Rad Biol Med 2009; 47: 1394-1400
  • 24 Lamb GD. Mechanisms of excitation-contraction uncoupling relevant to activity-induced muscle fatigue. Appl Physiol Nutr Metab 2009; 34: 368-372
  • 25 Langen RC, Schols AM, Kelders MC, Van Der Velden JL, Wouters EF, Janssen-Heininger YM. Tumor necrosis factor-alpha inhibits myogenesis through redox-dependent and -independent pathways. Am J Physiol 2002; 283: C714-C721
  • 26 LeBrasseur NK, Walsh K, Arany Z. Metabolic benefits of resistance training and fast glycolytic skeletal muscle. Am J Physiol 2011; 300: E3-E10
  • 27 Magherini F, Abruzzo PM, Puglia M, Bini L, Gamberi T, Esposito F, Veicsteinas A, Marini M, Fiorillo C, Gulisano M, Modesti A. Proteomic analysis and protein carbonylation profile in trained and untrained rat muscles. J Proteomics 2012; 75: 978-992
  • 28 Malek MH, Olfert IM, Esposito F. Detraining losses of skeletal muscle capillarization are associated with vascular endothelial growth factor protein expression in rats. Exp Physiol 2010; 95: 359-368
  • 29 Marini M, Lapalombella R, Margonato V, Ronchi R, Samaja M, Scapin C, Gorza L, Maraldi T, Carinci P, Ventura C, Veicsteinas A. Mild exercise training, cardioprotection and stress gene profile. Eur J Appl Physiol 2007; 99: 503-510
  • 30 McArdle A, Pattwell D, Vasilaki A, Griffiths RD, Jackson MJ. Contractile activity-induced oxidative stress: cellular origin and adaptive responses. Am J Physiol 2001; 280: C621-C627
  • 31 Musarò A, Fulle S, Fanò G. Oxidative stress and muscle homeostasis. Curr Opin Clin Nutr Metab Care 2010; 13: 236-242
  • 32 Phaneuf S, Leeuwenburgh C. Apoptosis and exercise. Med Sci Sports Exerc 2001; 33: 393-396
  • 33 Radak Z, Chung HY, Goto S. Systemic adaptation to oxidative challenge induced by regular exercise. Free Radic Biol Med 2008; 44: 153-159
  • 34 Renganathan M, Messi ML, Delbono O. Dihydropyridine receptor-ryanodine receptor uncoupling in aged skeletal muscle. J Membr Biol 1997; 157: 247-253
  • 35 Ristow M, Zarse K, Oberbach A, Klöting N, Birringer M, Kiehntopf M, Stumvoll M, Kahn CR, Blüher M. Antioxidants prevent health-promoting effects of physical exercise in humans. Proc Natl Acad Sci USA 2009; 106: 8665-8670
  • 36 Runchel C, Matsuzawa A, Ichijo H. Mitogen-activated protein kinases in mammalian oxidative stress responses. Antioxid Redox Signal 2011; 15: 205-218
  • 37 Sahlin K, Shabalina IG, Mattsson CM, Bakkman L, Fernström M, Rozhdestvenskaya Z, Enqvist JK, Nedergaard J, Ekblom B, Tonkonogi M. Ultraendurance exercise increases the production of reactive oxygen species in isolated mitochondria from human skeletal muscle. J Appl Physiol 2010; 108: 780-787
  • 38 Schiaffino S, Sandri M, Murgia M. Activity-dependent signaling pathways controlling muscle diversity and plasticity. Physiology 2007; 22: 269-278
  • 39 Spangenburg EE, Brown DA, Johnson MS, Moore RL. Alterations in peroxisome proliferator-activated receptor mRNA expression in skeletal muscle after acute and repeated bouts of exercise. Mol Cell Biochem 2009; 332: 225-231
  • 40 Staron RS, Kraemer WJ, Hikida RS, Fry AC, Murray JD, Campos GE. Fiber type composition of four hindlimb muscles of adult Fisher 344 rats. Histochem Cell Biol 1999; 111: 117-123
  • 41 Tupling AR, Vigna C, Ford RJ, Tsuchiya SC, Graham DA, Denniss SG, Rush JW. Effects of buthionine sulfoximine treatment on diaphragm contractility and SR Ca2+ pump function in rats. J Appl Physiol 2007; 103: 1921-1928
  • 42 Wilborn CD, Taylor LW, Greenwood M, Kreider RB, Willoughby DS. Effects of different intensities of resistance exercise on regulators of myogenesis. J Strength Cond Res 2009; 23: 2179-2187
  • 43 Yan Z, Okutsu M, Akhtar YN, Lira VA. Regulation of exercise-induced fiber type transformation, mitochondrial biogenesis, and angiogenesis in skeletal muscle. J Appl Physiol 2011; 110: 264-274
  • 44 Zorzano A, Palacín M, Gumà A. Mechanisms regulating GLUT4 glucose transporter expression and glucose transport in skeletal muscle. Acta Physiol Scand 2005; 183: 43-58