Int J Sports Med 2006; 27(1): 19-24
DOI: 10.1055/s-2005-837506
Physiology & Biochemistry

© Georg Thieme Verlag KG Stuttgart · New York

Alterations in Antioxidant Status, Protein Concentration, Acetylcholinesterase, Na+, K+-ATPase, and Mg2+-ATPase Activities in Rat Brain after Forced Swimming

T. Tsakiris1 , P. Angelogianni1 , C. Tesseromatis2 , S. Tsakiris1 , C. Tsopanakis1
  • 1Department of Experimental Physiology, Medical School, University of Athens, Athens, Greece
  • 2Department of Experimental Pharmacology, Medical School, University of Athens, Athens, Greece
Further Information

Publication History

Accepted after revision: November 25, 2004

Publication Date:
09 May 2005 (online)

Abstract

The aim of this study was to investigate whether exercise stress (short [2 h] or prolonged [5 h] forced swimming in rats) could modulate brain total antioxidant status (TAS), tissue protein concentration, and the activities of acetylcholinesterase (AChE), Na+, K+-ATPase, and Mg2+-ATPase. Protein concentration, TAS and enzyme activities in homogenized rat brain were determined spectrophotometrically. Protein concentration was decreased by 15 % (p < 0.01) and by 30 % (p < 0.001) after 2 h and 5 h of forced swimming, respectively. TAS was decreased by 20 - 25 % after 2 h or 5 h of exercise. AChE was inhibited by 30 % (p < 0.001) and 45 % (p < 0.001) after 2 h and 5 h of forced swimming, respectively. In contrast, Na+, K+-ATPase and Mg2+-ATPase were stimulated by 80 % (p < 0.001) and 40 % (p < 0.001), respectively, after 2 h of swimming and by 100 % (p < 0.001) and 60 % (p < 0.001), respectively, after 5 h of exercise. Control values in nontreated rats were unaltered (p > 0.05). In conclusion, short or prolonged forced swimming induces oxidative stress in rats, probably resulting in a reduction in brain protein concentration and AChE activity. In addition, a Na+, K+-ATPase and Mg2+-ATPase activation was observed under the above mentioned experimental conditions. This stress condition may modulate brain intracellular Mg2+ concentration, neural excitability, metabolic energy production, and neurotransmission.

References

  • 1 Alessio H M, Goldfarb A H, Cutler R G. MDA content increases in fast- and slow-twitch skeletal muscle with intensity of exercise in a rat.  Am J Physiol. 1988;  255 874-877
  • 2 Ames B N, Shinegawa M K, Hagen T M. Oxidants, antioxidants, and the degenerative diseases of aging.  Proc Natl Acad Sci USA. 1993;  90 7915-7922
  • 3 Beckman B, Ames B N. Oxidative decay of DNA.  J Biol Chem. 1997;  272 19633-19636
  • 4 Bogdanski D F, Tissuri A, Brodie B B. Role of sodium, potassium, ouabain and reserpine in uptake, storage and metabolism of biogenic amines in synaptosomes.  Life Sci. 1968;  7 419-428
  • 5 Bowler K, Tirri R. The temperature characteristics of synaptic membrane ATPases from immature and adult rat brain.  J Neurochem. 1974;  23 611-613
  • 6 Carageorgiou H, Tzotzes V, Pantos C, Mourousis C, Zarros A, Tsakiris S. In vivo and in vitro effects of cadmium on adult rat brain total antioxidant status, acetylcholinesterase, (Na+, K+)-ATPase and Mg2+-ATPase activities: Protection by L-cysteine.  Basic Clin Pharmacol Toxicol. 2004;  94 112-118
  • 7 Child R B, Wilkinson D M, Fallowfield J L, Donelly A E. Elevated serum antioxidant capacity and plasma malondialdehyde concentration in response to a simulated half-marathon run.  Med Sci Sports Exerc. 1998;  30 1603-1607
  • 8 Committee on Care and Use of Laboratory Animals .Guide for the Care and Use of Laboratory Animals. Washington, DC; Institute of Laboratory Animal Resources. National Research Council 1985: 83
  • 9 Cunningham H B, Yazaki P J, Domingo R C, Oades K V, Bohlen H, Sabbadini R A, Dahms A S. The skeletal muscle transverse tubular Mg-ATPase identity with Mg-ATPase of smooth muscle and brain.  Arch Biochem Biophys. 1993;  303 32-43
  • 10 Deliconstantinos G. Cortisol effect on (Na+, K+)-stimulated ATPase activity and on bilayer fluidity of dog brain synaptosomal plasma membranes.  Neurochem Res. 1985;  10 1605-1613
  • 11 Duthie G G, Robertson J D, Maughaman R J, Morrice C P. Blood antioxidant status and erythrocyte lipid peroxidation following distance running.  Arch Biochem Biophys. 1990;  282 78-83
  • 12 Ellman G L, Courtney D, Andres D, Featherstone R M. A new and rapid colorimetric determination of acetylcholinesterase activity.  Biochem Pharmacol. 1961;  7 88-95
  • 13 Fatranska M, Budai D, Oprsalova Z, Kretnansky R. Acetylcholine and its enzymes in some brain areas of the rat under stress.  Brain Res. 1987;  424 109-114
  • 14 Fujino K, Yoshitake T, Inoue O, Ibii N, Kehr J, Ishida J, Nohta H, Yamaguchi M. Increased serotonin release in mice frontal cortex and hippocampus induced by acute physiological stressors.  Neurosci Lett. 2002;  320 91-95
  • 15 Götz M E, Künig G, Riederer P, Youdim M BH. Oxidative stress: Free radical production in neural degeneration.  Pharmac Ther. 1994;  63 37-122
  • 16 Hermansen L, Hultman E, Saltin B. Muscle glycogen during prolonged severe exercise.  Acta Physiol Scand. 1967;  71 129-139
  • 17 Hernandez R. Brain Na+, K+-ATPase activity possibly regulated by a specific serotonin receptor.  Brain Res. 1987;  408 399-402
  • 18 Leeuwenburgh C, Hansen P, Shaish A, Holoszy J O, Heinrcke J W. Markers of protein oxidation by hydroxyl radical and reactive nitrogen species in tissues of aging rats.  Am J Physiol. 1998;  274 453-461
  • 19 Lowry O H, Rosebrough N J, Farr A L, Randall R J. Protein measurement with the folin phenol reagent.  J Biol Chem. 1951;  193 265-275
  • 20 Mata M, Fink D J, Gainer H, Smith C B, Davidsen L, Savakis H, Swartz W J, Sokoloff L. Activity-dependent energy metabolism in rat posterior pituitary primarily reflects sodium pump activity.  J Neurochem. 1980;  34 213-215
  • 21 Meyer E M, Cooper J R. Correlations between Na+, K+-ATPase activity and acetylcholine release in rat cortical synaptosomes.  J Neurochem. 1981;  36 467-475
  • 22 Molteni R, Fumagalli F, Magnaghi V, Roceri M, Gennaralli M, Racagni G, Melcangi R C, Riva M A. Modulation of fibroblast growth factor-2 by stress and corticosteroids: from developmental events to adult brain plasticity.  Brain Res Rev. 2001;  37 249-258
  • 23 Radak Z, Kaneko T, Tahara T, Nakamoto H, Ohno H, Sasvari M, Nyakas C, Goto S. The effect of exercise training on oxidative damage of lipids, proteins and DNA in rats skeletal muscle evidence for beneficial outcomes.  Free Radical Biol Med. 1999;  27 69-74
  • 24 Sanui H, Rubin H. The role of magnesium in cell proliferation and transformation. Boynton AL, McKeehan WL, Whitfield JF Ions, Cell Proliferation and Cancer. New York; Academic Press 1982: 517-537
  • 25 Sastry B SR, Phillis J W. Antagonism of biogenic amine-induced depression of cerebral cortical neurons by Na+, K+-ATPase inhibitors.  Can J Physiol Pharmacol. 1977;  55 170-180
  • 26 Schulpis K H, Tsakiris S, Karikas G A, Moukas M, Behrakis P. Effect of diet on plasma total antioxidant status in phenylketonuric patients.  Eur J Clin Nutr. 2003;  57 383-387
  • 27 Segal O L, Mats V N, Kruglikov R I. Changes in the protein level in rat hippocampal neurons during development of the alimentary conditioned reflex under normal conditions and after treatment with iproniazid.  Nauchnye Doki Vyss Shkoly Biol Nauki. 1987;  4 55-60
  • 28 Sen C K. Oxidants and antioxidants in exercise.  J Appl Physiol. 1995;  79 675-686
  • 29 Swann A C. Na+, K+-adenosine triphosphatase regulation by the sympathetic nervous system: effects of noradrenergic stimulation and lesion in vivo.  J Pharmacol Exp Ther. 1984;  228 304-311
  • 30 Sweadner K J, Goldin S M. Active transport of sodium and potassium ions: mechanism, function and regulation.  N Engl J Med. 1980;  302 777-783
  • 31 Tanaka M, Kohno Y, Nakagawa R, Ida Y, Takeda S, Nagasaki N. Time related differences in noradrenaline turnover in rat brain regions by stress.  Pharmacol Biochem Behav. 1982;  16 315-319
  • 32 Tanaka M, Kohno Y, Nakagawa R, Ida Y, Takeda S, Nagasaki N, Nada Y. Regional characteristics of stress-induced increases in brain noradrenaline release in rats.  Pharmacol Biochem Behav. 1983;  19 543-547
  • 33 Tsakiris S, Angelogianni P, Schulpis K H, Behrakis P. Protective effect of L-cysteine and glutathione on rat brain Na+, K+-ATPase inhibition induced by free radicals.  Z Naturforsch. 2000;  55C 271-277
  • 34 Tsakiris S. Effects of L-phenylalanine on acetylcholinesterase and Na+,K+-ATPase activities in adult and aged rat brain.  Mech Ageing Dev. 2001;  122 491-501
  • 35 Tsakiris S, Kontopoulos A N. Time changes in Na+, K+-ATPase, Mg2+-ATPase and acetylcholinesterase activities in the rat cerebrum and cerebellum caused by stress.  Pharmacol Biochem Behav. 1993;  44 339-342
  • 36 Tsakiris S, Koromilas C, Schulpis K H. Reduced Mg2+-ATPase activity in the hypoglycemic adult rat brain.  Z Naturforsch. 2001;  56C 912-914
  • 37 Tsakiris S, Schulpis K H, Tjamouranis J, Michelakakis H, Karikas G A. Reduced acetylcholinesterase activity in erythrocyte membranes from patients with phenylketonuria.  Clin Biochem. 2002;  35 615-619
  • 38 Tsakiris S, Schulpis K H, Marinou K, Behrakis P. Protective effect of L-cysteine and glutathione on the modulated suckling rat brain Na+, K+-ATPase and Mg2+-ATPase activities induced by the in vitro galactosaemia.  Pharmacol Res. 2004;  49 475-479
  • 39 Venditti P, Di Meo S. Antioxidants, tissue damage and endurance in trained and untrained young male rats.  Arch Biochem Biophys. 1996;  331 63-68
  • 40 Verditti P, Di Meo S. Effect of training on antioxidant capacity, tissue damage and endurance of adult male rats.  Int J Sports Med. 1997;  18 497-502
  • 41 Venditti P, Masullo P, Di Meo S. Effect of exercise duration on characteristics of mitochondrial population from rat liver.  Arch Biochem Biophys. 1999;  368 112-120
  • 42 Viggiano D, Vallone D, Ruocco L A, Sadile A G. Behavioural, pharmacological, morpho-functional molecular studies reveal a hyperfunctioning mesocortical dopamine system in an animal model of attention deficit and hyperactivity disorder.  Neurosci Biobehav Rev. 2003;  27 683-689
  • 43 Yamada K, Iida R, Miyamoto Y, Saito K, Sekikawa K, Seishima M, Nabeshima T. Neurobehavioral alterations in mice with a targeted deletion of the tumor necrosis factor-alpha gene: implications for emotional behavior.  J Neuroimmunol. 2000;  111 131-138

PhD S. Tsakiris

Department of Experimental Physiology, Medical School, University of Athens

P.O. Box 65257

15401 Athens

Greece

Fax: + 30 21 07 46 25 71

Email: stsakir@cc.uoa.gr

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