Sevil ARABACI TAMER, Özlem Tuğçe ÇİLİNGİR KAYA, Meral YÜKSEL, Alper YILDIRIM, Berrak Ç. YEĞEN

2210

A 10-day mild treadmill exercise performed before an epileptic seizure alleviates oxidative injury in the skeletal muscle and brain tissues of the rats

Objective: Epileptic seizures may cause skeletal muscle injury and memory dysfunctions. The present study was aimed to investigate the possible protective effects of exercising prior to seizure on seizure-induced oxidative injury in the skeletal muscle and brain. Materials and Methods: Sprague-Dawley male rats were assigned as non-exercise (n=16) and exercise groups (n=16). Following a 3-day exercise training, exercise protocol (30 min) was performed on a treadmill for 10 days, while control rats had no exercise. On the 11th day epileptic seizure was induced by a single intraperitoneal injection of pentylenetetrazol (PTZ) (45 mg/kg), while the control groups were injected with saline. Passive-avoidance test was initially performed before PTZ/saline injection and repeated 72 h later for the assessment of memory function. Brain and gastrocnemius muscles were taken for histological assessments and to determine the levels of malondialdehyde (MDA) and glutathione (GSH), myeloperoxidase (MPO) activity and luminal -and lucigenin- enhanced chemiluminescence levels. Results: Exercise training alone increased the formation of reactive oxygen species and elevated the antioxidant GSH capacity of the muscle tissue in the control rats, but these effects were not observed in the muscles of the exercised rats induced with a PTZ-seizure. On the other hand, short-term exercise alone had no effect on the basal oxidative parameters of the brain tissues. Prior exercise did not alter the average seizure scores or memory performances when compared to non-exercised groups, but suppressed the PTZ-induced elevations in MDA and chemiluminescence levels as well as MPO activity in the brain. Conclusion: A 10-day mild treadmill exercise reduced the oxidative brain damage due to a single seizure-induced excitotoxicity and exerted a preconditioning effect on the skeletal muscles exposed to tonic-clonic contractions.
Keywords:

Epileptic seizure, Exercise, Oxidative damage, Memory dysfunction, Skeletal muscle,

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  • Horváth L, Fekete I, Molnár M, Válóczy R, Márton S, Fekete K. The outcome of status epilepticus and long-term follow-up. Front Neurol 2019; 10:427-454. doi: 10.3389/fneur.2019.00427.
  • Zhen J, Qu Z, Fang H, et al. Effects of grape seed proanthocyanidin extract on pentylenetetrazole-induced kindling and associated cognitive impairment in rats. Int J Mol Med 2014; 34:391-8. doi: 10.3892/ijmm.2014.1796.
  • Mahmoudi T, Lorigooini Z, Rafieian-Kopaei M, et al. Effect of Curcuma zedoaria hydro-alcoholic extract on learning, memory deficits and oxidative damage of brain tissue following seizures induced by pentylenetetrazole in rat. Behav Brain Funct 2020; 16:1-12. doi: 10.1186/s12993-020-00169-3.
  • Nassiri-Asl M, Mortazavi S-R, Samiee-Rad F, et al. The effects of rutin on the development of pentylenetetrazole kindling and memory retrieval in rats. Epilepsy Behav 2010; 18:50-3. doi: 10.1016/j.yebeh.2010.03.005.
  • Power KN, Gramstad A, Gilhus NE, Hufthammer KO, Engelsen BA. Cognitive function after status epilepticus versus after multiple generalized tonic-clonic seizures. Epilepsy Res 2018; 140:39-45. doi: 10.1016/j.eplepsyres.2017.11.014.
  • Shulman MB, Barr W. Treatment of memory disorders in epilepsy. Epilepsy Behav 2002; 3:30-4. doi: 10.1016/S1525-5050(02)00509-7.
  • Sutter R, Dittrich T, Semmlack S, Rüegg S, Marsch S, Kaplan PW. Acute systemic complications of convulsive status Epilepticus—A systematic review. Crit Care Med 2018; 46:138-45. doi: 10.1097/CCM.0000000000002843.
  • Liguori R, Giannoccaro MP, Pasini E, et al. Acute rhabdomyolysis induced by tonic–clonic epileptic seizures in a patient with glucose-6-phosphate dehydrogenase deficiency. J Neurol 2013; 260:2669-71. doi: 10.1007/s00415-013-7103-z.
  • Malik GH. Rhabdomyolysis and myoglobin-induced acute renal failure. Saudi J Kidney Dis Transpl 1998; 9:273.
  • Nguyen R, Zenteno JFT. Injuries in epilepsy: a review of its prevalence, risk factors, type of injuries and prevention. Neurol Int 2009; 1:72-78. doi: 10.4081/ni.2009.e20.
  • Pandey S, Borah NC, Dwivedi M, Das RJ. Rhabdomyolysis with acute kidney injury after single episode of generalized seizure in a known case of epilepsy: a case report. Int J Res Med Sci 2020; 8:3757-60.
  • Arida RM. Physical exercise and seizure activity. Biochim Biophys Acta Mol Basis Dis 2020:165979. doi: 10.1016/j.bbadis.2020.165979.
  • Arida RM, de Almeida A-CG, Cavalheiro EA, Scorza FA. Experimental and clinical findings from physical exercise as complementary therapy for epilepsy. Epilepsy Behav 2013; 26:273-8. doi: 10.1016/j.yebeh.2012.07.025.
  • van den Bongard F, Hamer HM, Sassen R, Reinsberger C. Sport and physical activity in epilepsy: A systematic review. Dtsch Arztebl Int 2020; 117:1. doi: 10.3238/arztebl.2020.0001.
  • Gomes FN, Da Silva SG, Cavalheiro E, Arida R. Beneficial influence of physical exercise following status epilepticus in the immature brain of rats. Neuroscience 2014; 274:69-81. doi: 10.1016/j.neuroscience.2014.05.024.
  • Sartori CR, Pelágio FC, Teixeira SA, et al. Effects of voluntary running on spatial memory and mature brain-derived neurotrophic factor expression in mice hippocampus after status epilepticus. Behav Brain Res 2009; 203:165-72. doi: 10.1016/j.bbr.2009.04.022.
  • Campos DV, Lopim GM, de Almeida VS, Amado D, Arida RM. Effects of different physical exercise programs on susceptibility to pilocarpine-induced seizures in female rats. Epilepsy Behav 2016; 64:262-7. doi: 10.1016/j.yebeh.2016.08.011.
  • Setkowicz Z, Mazur A. Physical training decreases susceptibility to subsequent pilocarpine-induced seizures in the rat. Epilepsy Res 2006; 71:142-8. doi: 10.1016/j.eplepsyres.2006.06.002.
  • Ding YH, Young CN, Luan X, et al. Exercise preconditioning ameliorates inflammatory injury in ischemic rats during reperfusion. Acta Neuropathol 2005; 109:237-46. doi: 10.1007/s00401-004-0943-y.
  • Li F, Geng X, Huber C, Stone C, Ding Y. In search of a dose: The functional and molecular effects of exercise on post-stroke rehabilitation in rats. Front Cell Neurosci 2020; 14:186. doi: 10.3389/fncel.2020.00186.
  • Powers SK, Bomkamp M, Ozdemir M, Hyatt H. Mechanisms of exercise-induced preconditioning in skeletal muscles. Redox Biology 2020; 35:101462. doi: 10.1016/j.redox.2020.101462.
  • de Lima C, Arida RM, Andersen ML, et al. Effects of acute physical exercise in the light phase of sleep in rats with temporal lobe epilepsy. Epilepsy Res 2017; 136:54-61. doi: 10.1016/j.eplepsyres.2017.07.012.
  • Koyuncuoğlu T, Arabacı Tamer S, Erzik C, et al. Oestrogen receptor ERα and ERβ agonists ameliorate oxidative brain injury and improve memory dysfunction in rats with an epileptic seizure. Exp Physiol 2019; 104:1911-28. doi: 10.1113/EP087986.
  • Racine R, Okujava V, Chipashvili S. Modification of seizure activity by electrical stimulation: III. Mechanisms. Electroencephalogr Clin Neurophysiol 1972; 32:295-9. doi: 10.1016/0013-4694(72)90178-2.
  • Erşahin M, Toklu HZ, Erzik C, et al. The anti-inflammatory and neuroprotective effects of ghrelin in subarachnoid hemorrhage-induced oxidative brain damage in rats. J Neurotrauma 2010; 27:1143-55. doi: 10.1089/neu.2009.1210.
  • Elrod K, Buccafusco JJ. An evaluation of the mechanism of scopolamine-induced impairment in two passive avoidance protocols. Pharmacol Biochem Behav 1988; 29:15-21. doi: 10.1016/0091-3057(88)90267-5.
  • Bradley PP, Priebat DA, Christensen RD, Rothstein G. Measurement of cutaneous inflammation: estimation of neutrophil content with an enzyme marker. J Invest Dermatol 1982; 78:206-9. doi: 10.1111/1523-1747.ep12506462.
  • Tuğtepe H, Şener G, Bıyıklı NK, et al. The protective effect of oxytocin on renal ischemia/reperfusion injury in rats. Regul Pept 2007; 140:101-8. doi: 10.1016/j.regpep.2006.11.026.
  • Casini A, Ferrali M, Pompella A, Maellaro E, Comporti M. Lipid peroxidation and cellular damage in extrahepatic tissues of bromobenzene-intoxicated mice. Am J Pathol 1986; 123:520.
  • Aykaç G, Uysal M, Yalçin AS, Koçak-Toker N, Sivas A, Öz H. The effect of chronic ethanol ingestion on hepatic lipid peroxide, glutathione, glutathione peroxidase and glutathione transferase in rats. Toxicology 1985; 36:71-6. doi: 10.1016/0300-483x(85)90008-3.
  • Yildirim A, Tamer SA, Sahin D, et al. The effects of antibiotics and melatonin on hepato-intestinal inflammation and gut microbial dysbiosis induced by a short-term high-fat diet consumption in rats. Br J Nutr 2019; 122:841-55. doi: 10.1017/S0007114519001466.
  • Haklar G, Ulukaya‐Durakbaś Ç, Yüksel M, Dagh T, Yalcin A. Oxygen radicals and nitric oxide in rat mesenteric ischaemia‐reperfusion: Modulation by L‐arginine and NG‐nitro‐L‐arginine methyl ester. Clin Exp Pharmacol Physiol 1998; 25:908-12. doi: 10.1111/j.1440-1681.1998.tb02342.x.
  • Ahmad N, Welch I, Grange R, et al. Use of imaging biomarkers to assess perfusion and glucose metabolism in the skeletal muscle of dystrophic mice. BMC Musculoskelet Disord 2011; 12:127. doi: 10.1186/1471-2474-12-127.
  • Charge SB, Rudnicki MA. Cellular and molecular regulation of muscle regeneration. Physiol Rev 2004; 84:209-38. doi: 10.1152/physrev.00019.2003.
  • Hawke TJ, Garry DJ. Myogenic satellite cells: physiology to molecular biology. J Appl Physiol 2001. doi: 10.1152/jappl.2001.91.2.534.
  • Auer R, Kalimo H, Olsson Y, Siesjö B. The temporal evolution of hypoglycemic brain damage. II. Light-and electron-microscopic findings in the hippocampal gyrus and subiculum of the rat. Acta Neuropathol 1985; 67:25-36. doi: 10.1007/BF00688121.
  • Csordas A, Mazlo M, Gallyas F. Recovery versus death of" dark"(compacted) neurons in non-impaired parenchymal environment: light and electron microscopic observations. Acta Neuropathol 2003; 106:37-49. doi: 10.1007/s00401-003-0694-1.
  • Vasilev DS, Tumanova NL, Kim KK, et al. Transient morphological alterations in the hippocampus after pentylenetetrazole-induced seizures in rats. Neurochem Res 2018; 43:1671-82. doi: 10.1007/s11064-018-2583-y.
  • Volk T. Positioning nuclei within the cytoplasm of striated muscle fiber: cooperation between microtubules and KASH proteins. Nucleus (Calcutta) 2013; 4:18-22. doi: 10.4161/nucl.23086.
  • Kaminski RM, Rogawski MA, Klitgaard H. The potential of antiseizure drugs and agents that act on novel molecular targets as antiepileptogenic treatments. Neurotherapeutics 2014; 11:385-400. doi: 10.1007/s13311-014-0266-1.
  • Pimentel J, Tojal R, Morgado J. Epilepsy and physical exercise. Seizure 2015; 25:87-94. doi: 10.1016/j.seizure.2014.09.015.
  • Kayacan Y, Ghojebeigloo BE, Çerit G, Kocacan SE, Ayyıldız M. Physical exercise and 5-hydroxytryptophan, a precursor for serotonin synthesis, reduce penicillin-induced epileptiform activity. Epilepsy Behav 2020; 112:107403. doi: 10.1016/j.yebeh.2020.107403.
  • Arida RM, de Jesus Vieira A, Cavalheiro EA. Effect of physical exercise on kindling development. Epilepsy Res 1998; 30:127-32. doi: 10.1016/s0920-1211(97)00102-2.
  • McAuley JW, Long L, Heise J, et al. A prospective evaluation of the effects of a 12-week outpatient exercise program on clinical and behavioral outcomes in patients with epilepsy. Epilepsy Behav 2001; 2:592-600. doi: 10.1006/ebeh.2001.0271.
  • Arida RM, Scorza FA, Scorza CA, Cavalheiro EA. Is physical activity beneficial for recovery in temporal lobe epilepsy? Evidences from animal studies. Neurosci Biobehav Rev 2009; 33:422-31. doi: 10.1016/j.neubiorev.2008.11.002.
  • de Lima C, de Lira CAB, Arida RM, et al. Association between leisure time, physical activity, and mood disorder levels in individuals with epilepsy. Epilepsy Behav 2013; 28:47-51. doi: 10.1016/j.yebeh.2013.03.016.
  • Chen L, Gong S, Shan L-D, et al. Effects of exercise on neurogenesis in the dentate gyrus and ability of learning and memory after hippocampus lesion in adult rats. Neurosci Bull 2006; 22:1-6.
  • Devi PU, Manocha A, Vohora D. Seizures, antiepileptics, antioxidants and oxidative stress: an insight for researchers. Expert Opin Pharmacother 2008; 9:3169-77. doi: 10.1517/14656560802568230.
  • Kudin AP, Kudina TA, Seyfried J, et al. Seizure‐dependent modulation of mitochondrial oxidative phosphorylation in rat hippocampus. Eur J Neurosci 2002; 15:1105-14. doi: 10.1046/j.1460-9568.2002.01947.x.
  • Liu J, Wang A, Li L, Huang Y, Xue P, Hao A. Oxidative stress mediates hippocampal neuron death in rats after lithium–pilocarpine-induced status epilepticus. Seizure 2010; 19:165-72. doi: 10.1016/j.seizure.2010.01.010.
  • Sudha K, Rao AV, Rao A. Oxidative stress and antioxidants in epilepsy. Clin Chim Acta 2001; 303:19-24. doi: 10.1016/s0009-8981(00)00337-5.
  • Golechha M, Sarangal V, Bhatia J, Chaudhry U, Saluja D, Arya DS. Naringin ameliorates pentylenetetrazol-induced seizures and associated oxidative stress, inflammation, and cognitive impairment in rats: possible mechanisms of neuroprotection. Epilepsy Behav 2014; 41:98-102. doi: 10.1016/j.yebeh.2014.09.058.
  • Koyuncuoğlu T, Vızdıklar C, Üren D, et al. Obestatin improves oxidative brain damage and memory dysfunction in rats induced with an epileptic seizure. Peptides 2017; 90:37-47. doi: 10.1016/j.peptides.2017.02.005.
  • Lee S-J. Effects of preconditioning exercise on nitric oxide and antioxidants in hippocampus of epileptic seizure. Journal of Exercise Rehabilitation 2019; 15:757. doi: 10.12965/jer.1938698.349.
  • Mota BC, Pereira L, Souza MA, et al. Exercise pre-conditioning reduces brain inflammation and protects against toxicity induced by traumatic brain injury: behavioral and neurochemical approach. Neurotox Res 2012; 21:175-84. doi: 10.1007/s12640-011-9257-8.
  • Finaud J, Lac G, Filaire E. Oxidative stress. Sports Med 2006; 36:327-58. doi: 10.2165/00007256-200636040-00004.
  • Liu J, Yeo HC, Overvik-Douki E, et al. Chronically and acutely exercised rats: biomarkers of oxidative stress and endogenous antioxidants. J Appl Physiol 2000; 89:21-8. doi: 10.1152/jappl.2000.89.1.21.
  • Aoi W, Naito Y, Takanami Y, et al. Oxidative stress and delayed-onset muscle damage after exercise. Free Radic Biol Med 2004; 37:480-7. doi:10.1016/j.freeradbiomed.2004.05.008.
  • Morozov VI, Tsyplenkov PV, Golberg ND, Kalinski MI. The effects of high-intensity exercise on skeletal muscle neutrophil myeloperoxidase in untrained and trained rats. Eur J Appl Physiol 2006; 97:716-22. doi: 10.1007/s00421-006-0193-x.
  • Mehlhorn A, Strohm P, Hausschildt O, Schmal H, Sudkamp N. Seizure-induced muscle force can caused lumbar spine fracture. Acta Chir Orthop Traumatol Cech 2007; 74:202.
  • Mishra A, Dave N. Acute renal failure due to rhabdomyolysis following a seizure. J Family Med Prim Care 2013; 2:86-7. doi: 10.4103/2249-4863.109962.
Marmara Medical Journal-Cover
  • ISSN: 1019-1941
  • Yayın Aralığı: Yılda 3 Sayı
  • Başlangıç: 1988
  • Yayıncı: Marmara Üniversitesi
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