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Effect of a single session of electrical stimulation on activity and expression of citrate synthase and antioxidant enzymes in rat soleus muscle

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Abstract

The aim of our study was to investigate the effect of a single high intensity session of muscle contractions on the activity and expression of citrate synthase (CS) and of the following major antioxidant enzymes: Mn-superoxide dismutase (Mn-SOD), Cu,Zn-superoxide dismutase (Cu,Zn-SOD), catalase (CAT), and glutathione peroxidase (GPX). To accomplish this, soleus muscles of male Wistar rats were subjected to contractions using a intense electrical stimulation (ES) protocol. Soleus muscles were isolated either immediately or 1 h after the contractions and utilized for enzyme activity determination, and for analysis of gene expression by quantitative PCR. A significant increase in maximal activity (63%) and expression (80%) of CS was observed in stimulated soleus muscles, isolated 1 h after ES as compared to controls. However, this effect was not observed in muscles isolated immediately after ES. By using macroarray and Real Time RT-PCR analysis, an increase in expression of Mn-SOD, Cu,Zn-SOD, CAT, and GPX was also found. Interestingly, of these enzymes, only CAT activity was significantly increased (44%) 1 h after ES in soleus muscle. These results indicate that acute ES up-regulates activity and expression of CS and CAT in soleus muscles. This increase in expression of CAT may play an important role in counteracting the potential deleterious effects of elevated oxidative stress induced by a high oxidative demand in skeletal muscles subjected to exercise training.

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References

  • Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126

    PubMed  CAS  Google Scholar 

  • Atherton PJ, Babraj J, Smith K, Singh J, Rennie MJ, Wackerhage H (2005) Selective activation of AMPK-PGC-1alpha or PKB-TSC2-mTOR signaling can explain specific adaptive responses to endurance or resistance training-like electrical muscle stimulation. FASEB J 19(7):786–788

    PubMed  CAS  Google Scholar 

  • Beeckmans S (1984) Some structural and regulatory aspects of citrate synthase. Int J Biochem 16:341–351

    Article  PubMed  CAS  Google Scholar 

  • Braith RW, Magyari PM, Pierce GL, Edwards DG, Hill JA, White LJ, Aranda JM Jr (2005) Effect of resistance exercise on skeletal muscle myopathy in heart transplant recipients. Am J Cardiol 15; 95(10):1192–1198

    Google Scholar 

  • Booth FW, Thomason DB (1991) Molecular and cellular adaptation of muscle in response to exercise: perspectives of various models. Physiol Rev 71:541–585

    PubMed  CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  PubMed  CAS  Google Scholar 

  • Cooper MB, Jones DA, Edwards RH, Corbucci GC, Montanari G, Trevisani C (1986) The effect of marathon running on carnitine metabolism and on some aspects of muscle mitochondrial activities and antioxidant mechanisms. J Sports Sci 4:79–87

    PubMed  CAS  Google Scholar 

  • Fernstrom M, Tonkonogi M, Sahlin K (2004) Effects of acute and chronic endurance exercise on mitochondrial uncoupling in human skeletal muscle. J Physiol 554:755–763

    Article  PubMed  CAS  Google Scholar 

  • Flohe L, Otting F (1984) Superoxide dismutase assays. Methods Enzymol 105:93–104

    PubMed  CAS  Google Scholar 

  • Green H, Grant S, Bombardier E, Ranney D (1999) Initial aerobic power does not alter muscle metabolic adaptations to short-term training. Am J Physiol 277:E39–E48

    PubMed  CAS  Google Scholar 

  • Hainaut K, Duchateau J (1992) Neuromuscular electrical stimulation and voluntary exercise. Sports Med 14:100–113

    PubMed  CAS  Google Scholar 

  • Higuchi R, Dollinger G, Walsh PS, Griffith R (1992) Simultaneous amplification and detection of specific DNA sequences. Biotechnology (N Y) 10:413–417

    Article  CAS  Google Scholar 

  • Hollander J, Fiebig R, Gore M, Ookawara T, Ohno H, Ji LL (2001) Superoxide dismutase gene expression is activated by a single bout of exercise in rat skeletal muscle. Pflugers Arch 442:426–434

    Article  PubMed  CAS  Google Scholar 

  • Holloszy JO, Booth FW (1976) Biochemical adaptations to endurance exercise in muscle. Annu Rev Physiol 38:273–291

    Article  PubMed  CAS  Google Scholar 

  • Holloszy JO, Oscai LB, Don IJ, Mole PA (1970) Mitochondrial citric acid cycle and related enzymes: adaptive response to exercise. Biochem Biophys Res Commun 40:1368–1373

    Article  PubMed  CAS  Google Scholar 

  • Itoh M, Oh-Ishi S, Hatao H, Leeuwenburgh C, Selman C, Ohno H, Kizaki T, Nakamura H, Matsuoka T (2004) Effects of dietary calcium restriction and acute exercise on the antioxidant enzyme system and oxidative stress in rat diaphragm. Am J Physiol Regul Integr Comp Physiol 287:R33–R38

    PubMed  CAS  Google Scholar 

  • Jacobs I, Esbjornsson M, Sylven C, Holm I, Jansson E (1987) Sprint training effects on muscle myoglobin, enzymes, fiber types, and blood lactate. Med Sci Sports Exerc 19:368–374

    PubMed  CAS  Google Scholar 

  • Ji LL, Dillon D, Wu E (1990) Alteration of antioxidant enzymes with aging in rat skeletal muscle and liver. Am J Physiol 258:R918–R923

    PubMed  CAS  Google Scholar 

  • Ji LL, Fu R (1992) Responses of glutathione system and antioxidant enzymes to exhaustive exercise and hydroperoxide. J Appl Physiol 72:549–554

    PubMed  CAS  Google Scholar 

  • Ji LL, Fu R, Mitchell EW (1992) Glutathione and antioxidant enzymes in skeletal muscle: effects of fiber type and exercise intensity. J Appl Physiol 73:1854–1859

    PubMed  CAS  Google Scholar 

  • Ji LL, Stratman FW, Lardy HA (1988) Enzymatic down regulation with exercise in rat skeletal muscle. Arch Biochem Biophys 263:137–149

    Article  PubMed  CAS  Google Scholar 

  • Khassaf M, Child RB, McArdle A, Brodie DA, Esanu C, Jackson MJ (2001) Time course of responses of human skeletal muscle to oxidative stress induced by nondamaging exercise. J Appl Physiol 90:1031–1035

    PubMed  CAS  Google Scholar 

  • Lawler JM, Powers SK, Van Dijk H, Visser T, Kordus MJ, Ji LL (1994) Metabolic and antioxidant enzyme activities in the diaphragm: effects of acute exercise. Respir Physiol 96:139–149

    Article  PubMed  CAS  Google Scholar 

  • Lawler JM, Powers SK, Visser T, Van Dijk H, Kordus MJ, Ji LL (1993) Acute exercise and skeletal muscle antioxidant and metabolic enzymes: effects of fiber type and age. Am J Physiol 265:R1344–R1350

    PubMed  CAS  Google Scholar 

  • Leek BT, Mudaliar SR, Henry R, Mathieu-Costello O, Richardson RS (2001) Effect of acute exercise on citrate synthase activity in untrained and trained human skeletal muscle. Am J Physiol Regul Integr Comp Physiol 280:R441–R447

    PubMed  CAS  Google Scholar 

  • Leeuwenburgh C, Fiebig R, Chandwaney R, Ji LL (1994) Aging and exercise training in skeletal muscle: responses of glutathione and antioxidant enzyme systems. Am J Physiol 267:R439–R445

    PubMed  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25:402–408

    Article  PubMed  CAS  Google Scholar 

  • Navarro-Arevalo A, Canavate C, Sanchez-del-Pino MJ (1999) Myocardial and skeletal muscle aging and changes in oxidative stress in relationship to rigorous exercise training. Mech Ageing Dev 108:207–217

    Article  PubMed  CAS  Google Scholar 

  • Nader GA, Esser KA (2001) Intracellular signaling specificity in skeletal muscle in response to different modes of exercise. J Appl Physiol 90(5):1936–1942

    PubMed  CAS  Google Scholar 

  • Neufer PD, Dohm GL (1993) Exercise induces a transient increase in transcription of the GLUT-4 gene in skeletal muscle. Am J Physiol 265:C1597–C1603

    PubMed  CAS  Google Scholar 

  • Oh-ishi S, Kizaki T, Nagasawa J, Izawa T, Komabayashi T, Nagata N, Suzuki K, Taniguchi N, Ohno H (1997) Effects of endurance training on superoxide dismutase activity, content and mRNA expression in rat muscle. Clin Exp Pharmacol Physiol 24:326–332

    Article  PubMed  CAS  Google Scholar 

  • Ohishi S, Kizaki T, Ookawara T, Toshinai K, Haga S, Karasawa F, Satoh T, Nagata N, Ji LL, Ohno H (1998) The effect of exhaustive exercise on the antioxidant enzyme system in skeletal muscle from calcium-deficient rats. Pflugers Arch 435:767–774

    Article  PubMed  CAS  Google Scholar 

  • Ortenblad N, Madsen K, Djurhuus MS (1997) Antioxidant status and lipid peroxidation after short-term maximal exercise in trained and untrained humans. Am J Physiol 272:R1258–R1263

    PubMed  CAS  Google Scholar 

  • Ramakers C, Ruijter JM, Deprez RH, Moorman AF (2003) Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci Lett 339:62–66

    Article  PubMed  CAS  Google Scholar 

  • Roepstorff C, Schjerling P, Vistisen B, Madsen M, Steffensen CH, Rider MH, Kiens B (2005) Regulation of oxidative enzyme activity and eukaryotic elongation factor 2 in human skeletal muscle: influence of gender and exercise. Acta Physiol Scand 184:215–224

    Article  PubMed  CAS  Google Scholar 

  • Sahlin K, Ren JM (1989) Relationship of contraction capacity to metabolic changes during recovery from a fatiguing contraction. J Appl Physiol 67:648–654

    PubMed  CAS  Google Scholar 

  • Sambrook LE, Fritisch EF, Maniatis T (2001) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  • Silveira LR, Hirabara SM, Alberici LC, Lambertucci RH, Peres CM, Takahashi HK, Pettri A, Alba-Loureiro T, Luchessi AD, Cury-Boaventura MF, Vercesi AE, Curi R (2007) Effect of lipid infusion on metabolism and force of rat skeletal muscles during intense contractions. Cell Physiol Biochem 20(1–4):213–226

    PubMed  CAS  Google Scholar 

  • Siu PM, Donley DA, Bryner RW, Alway SE (2003) Citrate synthase expression and enzyme activity after endurance training in cardiac and skeletal muscles. J Appl Physiol 94:555–560

    PubMed  CAS  Google Scholar 

  • Spina RJ, Chi MM, Hopkins MG, Nemeth PM, Lowry OH, Holloszy JO (1996) Mitochondrial enzymes increase in muscle in response to 7–10 days of cycle exercise. J Appl Physiol 80:2250–2254

    PubMed  CAS  Google Scholar 

  • Srere PA, Brazil H, Gonen L (1963) The citrate condensing enzyme of pigeon breast muscle and moth flight muscle. Acta Chemica Scandinavica 17:129–134

    Google Scholar 

  • 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(5):495–501

    Article  PubMed  CAS  Google Scholar 

  • Tonkonogi M, Harris B, Sahlin K (1997) Increased activity of citrate synthase in human skeletal muscle after a single bout of prolonged exercise. Acta Physiol Scand 161:435–436

    Article  PubMed  CAS  Google Scholar 

  • Verlengia R, Gorjao R, Kanunfre CC, Bordin S, de Lima TM, Martins EF, Newsholme P, Curi R (2004) Effects of EPA and DHA on proliferation, cytokine production, and gene expression in Raji cells. Lipids 39:857–864

    Article  PubMed  CAS  Google Scholar 

  • Vissing K, Andersen JL, Schjerling P (2005) Are exercise-induced genes induced by exercise? Faseb J 19:94–96

    PubMed  CAS  Google Scholar 

  • Wendel A (1981) Glutathione peroxidase. Methods Enzymol 77:325–333

    Article  PubMed  CAS  Google Scholar 

  • Wiegand G, Remington SJ (1986) Citrate synthase: structure, control, and mechanism. Annu Rev Biophys Biophys Chem 15:97–117

    Article  PubMed  CAS  Google Scholar 

  • Wojtaszewski JF, Hansen BF, Urso B, Richter EA (1996) Wortmannin inhibits both insulin- and contraction-stimulated glucose uptake and transport in rat skeletal muscle. J Appl Physiol 81:1501–1509

    PubMed  CAS  Google Scholar 

  • Yamazaki K, Kuromitsu J, Tanaka I (2002) Microarray analysis of gene expression changes in mouse liver induced by peroxisome proliferator- activated receptor alpha agonists. Biochem Biophys Res Commun 290:1114–1122

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

The authors are indebted to the constant technical assistance of E. P. Portiolli, T. C. Alba, J. R. Mendonça, and G. de Souza. This study is supported by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP), and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES).

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  1. Department of Physiology and Biophysics, Institute of Biomedical Sciences, University of São Paulo, Avenida Professor Lineu Prestes 1524, sala 105 Butantan, 05508-900, São Paulo, SP, Brazil

    Aurélio da Silva Pimenta, Rafael Herling Lambertucci, Renata Gorjão, Leonardo dos Reis Silveira & Rui Curi

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  1. Aurélio da Silva Pimenta
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  2. Rafael Herling Lambertucci
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  3. Renata Gorjão
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  4. Leonardo dos Reis Silveira
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Correspondence to Rui Curi.

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da Silva Pimenta, A., Lambertucci, R.H., Gorjão, R. et al. Effect of a single session of electrical stimulation on activity and expression of citrate synthase and antioxidant enzymes in rat soleus muscle. Eur J Appl Physiol 102, 119–126 (2007). https://doi.org/10.1007/s00421-007-0542-4

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